Brain and Language 98 (2006) 40–56

www.elsevier.com/locate/b&l

Cortical memory mechanisms and language origins

Francisco Aboitiz ¤, Ricardo R. García, Conrado Bosman, Enzo Brunetti

Depto. Psiquiatría, Facultad de Medicina, PontiWcia Universidad Católica de Chile, Marcoleta no. 387 2o piso, Casilla 114-D Santiago 1, Chile

Accepted 12 January 2006Available online 14 February 2006

Abstract

We have previously proposed that cortical auditory-vocal networks of the monkey brain can be partly homologized with languagenetworks that participate in the phonological loop. In this paper, we suggest that other linguistic phenomena like semantic and syntacticprocessing also rely on the activation of transient memory networks, which can be compared to active memory networks in the primate.Consequently, short-term cortical memory ensembles that participate in language processing can be phylogenetically tracked to moresimple networks present in the primate brain, which became increasingly complex in hominid evolution. This perspective is discussed inthe context of two current interpretations of language origins, the “mirror-system hypothesis” and generativist grammar.© 2006 Elsevier Inc. All rights reserved.

Keywords: Broca’s area; Mirror neurons; Syntax; Wernicke’s area; Working memory

1. Introduction

In the last decade, there has been a growing interest inshort-term memory phenomena that maintain the neuronalactivation related to perceptual or long-term mnemonicitems, in order to execute a near-future response (Fuster,1995a; Fuster & Alexander, 1971; Levy & Goldman-Rakic,2000). In humans, this kind of memory has been termedworking memory (Baddeley, 1992; Baddeley & Hitch,1974), and has been proposed to participate in several cog-nitive mechanisms, including language acquisition and pro-cessing (Baddeley, 1992, 2000, 2003; Baddeley, Papagno, &Vallar, 1988; Caplan, Alpert, & Waters, 1998; Caplan,Alpert, Waters, & Olivieri, 2000; Fiebach, Schelewsky, &Friederici, 2002; Fiebach, Schlesewsky, Lohmann, von Cra-mon, & Friederici, 2005; Gathercole & Baddeley, 1990;Gibson, 1998; Just & Carpenter, 1992; King & Kutas, 1995;Müller & Basho, 2004). Furthermore, cognitive and neuro-biological evidence suggests that the distinct aspects of lan-guage processing, including phonological, lexical, semantic,

* Corresponding author. Fax: +56 2 665 1951.E-mail address: faboitiz@puc.cl (F. Aboitiz).URL: http://www.neuro.cl (F. Aboitiz).

0093-934X/$ - see front matter © 2006 Elsevier Inc. All rights reserved.doi:10.1016/j.bandl.2006.01.006

and syntactic domains, all rely importantly on short-termmemory mechanisms (Bookheimer, 2002; Caplan &Waters, 1999; Hickock & Poeppel, 2000; Lieberman, 2002).

Working memory has been classically subdivided into ageneral, all-purpose executive system that manipulates themnemonic items, and “slave” systems involved in sensori-motor rehearsal. The latter have been further subdividedinto a visuospatial sketchpad, which maintains online visu-ospatial information, and a phonological loop, that allowsinternal rehearsal of phonological utterances (Baddeley &Hitch, 1974). SpeciWcally, in humans, the phonological loophas been anatomically identiWed (see below) and shown tobe important for language learning. For example, patientswith phonological working memory deWcits show impair-ments in long-term phonological learning, and a link hasbeen observed between performance in the phonologicalloop and vocabulary level in children (Baddeley et al., 1988;Gathercole & Baddeley, 1990). Furthermore, speciWc lan-guage impairment, a developmental condition character-ized by deWcits in language learning, appears to have as acentral characteristic a phonological working memory dys-function (Webster & Shevell, 2004). According to Baddeley(2000), this evidence suggests that the loop might haveevolved to enhance language acquisition.

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 41

However, cortical short-term memory mechanisms aremore diverse and involve other modalities or sensorimotordomains than the phonological loop and the visuospatialsketchpad (Fuster, 1995a). Furthermore, certain higher-level cognitive phenomena such as attention also implyshort-term memory mechanisms that do not exactly Wt theconcept of “slave” sensorimotor systems (de Fockert, Rees,Frith, & Lavie, 2001). Although the concept of a centralexecutive that distributes resources in diVerent processingdomains might adequately grasp some of these phenomena,the anatomical localization of this system in the dorsolat-eral prefrontal cortex has been questioned by some authors(Goldman-Rakic, 1996, 2000). Partly for this reason, weconsider that the more general, neurophysiological conceptof active memory (Fuster, 1995a; Fuster & Alexander,1971) may be more appropriate in this context. This termimplies “a broad network of associative memory” which ismaintained “as a perceptual memory fragment in order toexecute a motor act in the near future” (Fuster, 1995b,p. 64). In other words, active memory is a property of neu-ronal ensembles that consists of the capacity to maintain anactivated state during the execution of a cognitive task, thusholding information online for a brief time interval (Fuster,1995a, 1995b). Nevertheless, more than being speciWc mem-ory circuits, the above networks are elements that link sen-sory and motor domains in the context of near-futurebehavior. Furthermore, the fact that active memory ensem-bles are associative as Fuster proposes implies that they arechangeable, plastic, and that these overlap and interact withother active networks during the preparation and executionof complex behaviors, thus generating larger ensemblesmanipulating more than one memory item (for a more for-mal analysis, see Glassman, 2003). The mechanisms bywhich these networks maintain their activated state are notyet clear, but an intriguing possibility is that they do sothrough the establishment of reciprocally connected ensem-bles which oscillate synchronously (Engel, Fries, & Singer,2001; Singer, 1999; Durstewitz, Seamans, & Sejnowski,2000; Yuste, MacLean, Smith, & Lansner, 2005). There isaccumulating evidence indicating that neural synchronywith a precision in the millisecond range participates in sev-eral cognitive phenomena including working memory, in amanner consistent with Hebb’s postulate of maintainedreciprocal activation. These studies show that short-termstorage mechanisms involve an increase in neural syn-chrony between prefrontal cortex and posterior cortex,together with enhancing the activation of long-term mem-ory representations (Engel & Singer, 2001; Fingelkurtset al., 2003; Palva, Palva, & Kaila, 2005; Ruchkin, Graf-man, Cameron, & Berndt, 2003; Tallon-Baudry, Bertrand,& Fischer, 2001; Tallon-Baudry, Mandon, Freiwald, &Kreiter, 2004).

In this article, we propose (1) that the neural circuits thatparticipate in the phonological loop can be anatomicallydescribed in incipient form in the non-human primatebrain, and that therefore these are homologous to thehuman circuits (Aboitiz, 1995; Aboitiz & García, 1997);

and (2) that in part, language has evolved by virtue of anexpanding short-term memory capacity, which has allowedthe processing and manipulation of increasingly complexsequences of sounds, conveying elaborate meanings andeventually participating in syntactic processes. Thus, thelanguage-speciWc areas of the human brain may have ini-tially evolved as a circuit for phonological rehearsalinvolved in learning relatively long phonological utter-ances, which became conventionalized and acquired simplemeanings by associative interactions with other sensorimo-tor domains. As the memory systems involved in this pro-cess expanded, it became possible to activate more complexmemories representing several items that could be combi-natorially manipulated (Glassman, 2003). This allowedutterances and their meanings to become also increasinglycomplex and speciWc. Eventually, primitive syntactic rulesappeared within the context of a highly intricate short-termmemory network that allowed to maintain previously per-ceived lexical items on line while others were still being pro-cessed. Although intuitively appealing, this proposal facesother recent hypotheses. One of them is the “mirror-sys-tem” hypothesis, which emphasizes the role of hand-grasp-ing mirror neurons in language origins (Arbib & Bota,2003; Rizzolatti & Arbib, 1998). Shortly, the hypothesissuggests that the manual mirror-neuron system providedthe necessary plasticity for symbolic communication toarise in a gestural domain, which was eventually overcomeby vocal communication. Although we feel that the conceptof mirror neurons is in general complementary to ourviews, there are some points of disagreement which we willdiscuss. Another proposal relates to Chomsky’s generativistapproach which claims that syntax, and speciWcally theoperation termed syntactic recursion (i.e., the ability torecursively embed sentences within larger sentences; seebelow), is the only faculty that is exclusive of human lan-guage and unlikely to result from evolution by naturalselection (see Hauser, Chomsky, & Fitch, 2002). We claimthat linguistic recursion demands signiWcant working mem-ory resources, and that at least partly, neural networks thatparticipate in recursion were gradually elaborated fromsimpler networks involved in active memory in the primatebrain.

In the rest of the article, we will discuss evidence in favorof our hypothesis. We will brieXy update evidence on thelocation and connectivity of the human language areas andof the phonological loop, and their presumed homologuesin the monkey. Then, we will face this evidence with themirror-system hypothesis. Finally, we will analyze the roleof short-term memory in syntactical processing, especiallyin the case of recursive structures, and will propose a neuro-biological substrate for it and its evolution.

2. Neuroanatomy of phonological working memory and homologies between monkey and human

More than a century of analyses of focalized brainlesions in humans has evidenced that cortical language

42 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

networks minimally consist of a posterior component sur-rounding the temporoparietal junction of the left hemi-sphere (Wernicke’s area), that mediates speech perceptionand aspects of phonological production; an anterior com-ponent that includes Brodmann’s areas 44 and 45 orBroca’s area, which processes motor output and aspectsof syntax, and a connection between these two compo-nents, which includes the arcuate fasciculus (althoughimportantly, surrounding regions also participate; Dron-kers, Shapiro, Redfern, & Knight, 1992; Dronkers, Wil-kins, Van Valin, Redfern, & Jaeger, 2004). This schemehas been conWrmed and expanded by analyses of stimula-tion brain mapping which have established that regionsessential for language processing are usually restricted toone hemisphere and tend to locate in temporal, inferiorparietal and inferior frontal areas (although there is sub-stantial variance in individual patterns of localization;Ojemann, 1991, 2003), and by several imaging studies tobe reviewed below. In earlier articles (Aboitiz, 1995; Abo-itiz & García, 1997), we tentatively proposed a frameworkfor homology between the classical human language areasand their primate counterparts, based on the available evi-dence at that time (for example, Barbas & Pandya, 1989;Preuss & Goldman-Rakic, 1991a, 1991b, 1991c), whichhas been recently updated according to new evidence(Aboitiz, García, Brunetti, & Bosman, in press) (seeFig. 1).

The auditory cortex, both in the human and themacaque, is organized in a series of concentric rings (core,belt, and parabelt; Hackett, Stepniewska, & Kaas, 1998)

Fig. 1. Some connections that have been described from temporoparietalregions to the lateral and inferior frontal cortex of the monkey. In thesuperior temporal lobe, areas AI, R, and RT of the auditory cortex makeup the auditory core, while areas RTM, RM, and CM correspond to themedial belt and areas RTL, AL, ML, and CL represent the lateral belt.The lateral parabelt consists of areas RP and CP, while area Tpt may beadjacent to these. The caudal parabelt projects to dorsolateral prefrontalareas, while the rostral parabelt projects to ventrolateral prefrontalregions. Area TE, in the anterior temporal lobe, is related to visual recog-nition and projects to ventral lateral cortex. In the intraparietal and infe-rior parietal lobe, areas 7ip and 7b, respectively, project to ventrolateralregions of the frontal cortex, among other regions. Numbers in the frontalcortex indicate the respective Brodmann’s areas. For further explanation,see text.

from which two main streams emerge: a ventral one, run-ning through the anterior superior temporal gyrus, con-veying information about the intrinsic features of auditorystimuli (the “what” pathway); and a dorsal one, projectingto the inferior parietal lobe and involved with spatial anddynamic processing (the “where,” or movement pathway;Kaas & Hackett, 1999; Tian, Reser, Durham, Kustov, &Rauschecker, 2001; Zatorre & Belin, 2001). These twopathways project to diVerent regions of the prefrontal cor-tex: in the macaque, the “where” pathway ends mainly indorsolateral prefrontal areas (areas 8 and 46) which in partrelate to eye movement control; and the “what” pathwayends in more ventrolateral areas (mainly 12 and 45, the lat-ter related to Broca’s area in humans; Hackett, Step-niewska, & Kaas, 1999; Rauschecker & Tian, 2000;Romanski, Tian, Mishkin, Goldman-Rakic, & Raushec-ker, 1999; Romanski, Bates, & Goldman-Rakic, 1999).There is evidence indicating that these temporo-frontalcircuits subserve performance in auditory working mem-ory tasks (Gottlieb, Vaadia, & Abeles, 1989; Pasternak &Greenlee, 2005). Interestingly, an auditory domain hasbeen identiWed in the macaque areas 12 and 45, in whichmost neurons prefer vocalizations than other acousticstimuli, while some neurons were also responsive to visualstimuli (Romanski & Goldman-Rakic, 2002; Romanski,Averbeck, & Diltz, 2005). This domain receives projectionsfrom the anterior lateral belt auditory area, which hasmore selectivity to calls than the more caudal area (Raus-checker & Tian, 2000; Tian et al., 2001). In this region, aspecialization of “what” and “where” streams in responsesto complex sounds and localizations has not been yet con-Wrmed (Romanski et al., 2005), and it remains to be deter-mined whether the dorsal stream contributes a diVerentauditory domain in more dorsal frontal regions. Anotherline of evidence has been provided by Petrides and Pandya(1984, 1988, 1999, 2001; see also Petrides, in press), whoproposed a similar scheme to the above, in which area 45 issubdivided into areas 45A and 45B, and describe a dys-granular area 44, adjacent to area 45B. Nevertheless, theseauthors describe some projections from caudal auditoryregions (for example, area Tpt) to ventrolateral prefrontalareas, indicating a degree of overlap between the “where”and “what” streams (Petrides & Pandya, 1988).

In parallel to the auditory “what” and “where” path-ways, the visual system shows a separation between a ven-tral stream along the inferior temporal lobe, related toobject processing; and a dorsal stream directed to the parie-tal lobe, that is related to spatial behavior. These pathwaystend to segregate in the inferior and superior aspects of thefrontal lobe, respectively (Bullier, Schall, & Morel, 1996;Felleman & Van Essen, 1991). Nevertheless, projectionsfrom the inferior parietal regions reach the inferior frontalcortex of the monkey, where they converge with projectionsfrom inferior temporal areas subserving object information(Fig. 1). More speciWcally, the intraparietal (area 7ip) andinferior parietal (area 7b) regions project to the anteriorand the posterior banks of the inferior arcuate sulcus,

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 43

respectively (Cavada & Goldman-Rakic, 1989; Petrides &Pandya, 1984; Preuss & Goldman-Rakic, 1991a, 1991b,1991c). Similarly, Petrides and Pandya (1984, 1999, 2001;see also Petrides, in press) emphasize connections betweenarea 45 with the posterior inferior parietal lobe (area PG)and area 44 with the intraparietal and anterior inferiorparietal lobe (areas AIP and PFG, respectively). Note thatperhaps more than spatial processing in the context ofbehavioral orientation, inferior parietal regions participatein tasks involving grasping and object manipulation (Riz-zolatti & Arbib, 1998; see below). Their projections to theinferior frontal lobe overlap with the object-processingpathway from the inferior temporal lobe, contributing tothe integration of information between hand and object(Nelissen, Luppino, VanduVel, Rizzolatti, & Orban, 2005).As will be seen below, although the auditory dorsal path-way (as said, roughly parallel to the visual parietal path-way) is less likely to be involved in manipulative tasks, itparticipates in processing the temporal dynamics of com-plex sounds, which make it somewhat analogous to themotion-sensitive regions of the parietal lobe.

In humans, a dorsal and a ventral stream for processingsounds have also been identiWed (Belin & Zatorre, 2000;Zatorre & Belin, 2001; see also Scott & Johnsrude, 2003). Inspeech perception, the ventral stream participates in identi-fying the speaker, while the dorsal stream is considered tobe primarily involved in perceiving the time-course of com-plex sounds, a mechanism based on accurate time analysisof spectral motion. This process might seem to be morerelated to the “what” function of categorizing sounds, butthese authors claim that it is analogous to the function ofthe motion-sensitive visual parietal area MT, in that thetime-course of the signal is an essential variable (Belin &Zatorre, 2000; Zatorre & Belin, 2001). More than identify-ing the speaker, this type of processing is especially wellsuited to process complex vocalization sequences whichreXect motion of the vocal apparatus, and particularlyspeech, where the time-course of the formant frequenciescontains most of the phonemic information. Romanskiet al. (2000) concur with these authors in that this generalform of ‘motion processing’ mechanism may be one of thefunctions of the dorsal pathway, but can be used in serviceof both auditory space perception and the perception ofcomplex vocalizations. Additional evidence indicates thatthe temporal pathway for speech perception is subdividedinto a component directed along the supratemporal corticalplane and linked to speech production rather than percep-tion; and a component located in the posterior left superiortemporal sulcus, related to verbal recall (Wise et al., 2001).The latter is considered to participate in verbal generationand rehearsal (the phonological loop), and has been pro-posed to participate in the acquisition of long-term memo-ries of novel words. Finally, a recent study using diVusionMRI tractography in humans detected both a ventral path-way (via the uncinate fasciculus) and a dorsal pathway (viathe arcuate fasciculus and including connections with area40 in the supramarginal gyrus), connecting the auditory

areas with the inferior frontal lobe (Parker et al., 2005).Interestingly, these tracts were highly asymmetric, beingmore robust on the left side.

Summarizing, the ventrolateral prefrontal region of themonkey, including areas 44/45 (comparable to Broca’sarea), is a complex multimodal region receiving projectionsfrom the auditory “what” stream (but also some projec-tions from the “where” stream), from the inferior temporalregion and from intraparietal/inferior parietal areas(Fig. 1). In humans, anatomically similar regions have beendescribed to participate in the phonological loop, whichsubserves phonological working memory. This loop hasbeen described to include a storage component located inthe left supramarginal gyrus of the inferior parietal lobe(Brodmann’s area 40), and a rehearsal component involv-ing Broca’s area (areas 44 and 45; Awh, Smith, & Jonides,1995; Frackowiak, 1994; Habib, Demonet, & Frackowiak,1996; Hickok, Buchsbaum, Humphries, & Muftuler, 2003;Paulesu, Frith, & Frackowiak, 1993; Salmon et al., 1996;see also reviews by Aboitiz & García, 1997; Baddeley, 2003;Smith & Jonides, 1998). This is consistent with a recentanalysis of human cortical connectivity, indicating impor-tant connections between Wernicke’s area and area 40(Parker et al., 2005). More extensive evidence from lesionstudies has conWrmed that parietal lesions in humans leadto sentence comprehension deWcits, by virtue of a rehearsaldisorder related to the interruption of the parieto-frontalphonological loop, as occurs in conduction aphasia (Dron-kers et al., 2004; see also Aboitiz & García, 1997; Smith &Jonides, 1998). Furthermore, electrical stimulation brainmapping techniques during awake neurosurgery havedetermined that sites essential for recent verbal memory ofnames tend to be located in temporo-parietal sites (relatedwith storage) and in inferior frontal sites (related withretrieval) (Ojemann, 1978, 1991, 2003; Ojemann & Mateer,1979).

Based on this kind of evidence, we proposed that the supe-rior temporal–inferior parietal–ventrolateral prefrontal path-way that participates in the phonological loop could beincipiently present in the non-human primate. In hominidevolution, this pathway may have further diVerentiated intoa complex phonological device, involved in learning complexvocal utterances by imitation and setting a Wrst stage in thediVerentiation of language-speciWc areas in the left hemi-sphere of the human brain (Aboitiz, 1995; Aboitiz & García,1997; see also Fitch, 2000). The ventral auditory stream pos-sibly represents a more ancient component of the vocaliza-tion sensorimotor system, whose main function could be toidentify and assess the condition of the caller. As mentioned,recent evidence suggests that in macaques this pathway ismore related to vocalizations than the dorsal stream, whichparticipates in spatial orienting for action (Romanski et al.,2005). However, in primitive hominids in which vocalizationsbecame more plastic and conveyed longer and more elabo-rate messages, the dorsal stream became progressivelyinvolved in processing complex sequences of vocalizations,recruiting inferior parietal areas (Aboitiz & García, 1997).

44 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

The occipito-temporoparietal junction is an evolutionarilyexpanding cortical region, and its growth may have facili-tated the development of the dorsal auditory pathway andthe phonological loop. SpeciWcally, areas 40 and 39 of thehuman inferior parietal lobe are probably new in phylogeny,as they were not identiWed in the monkey (Brodmann, 1909).(Nevertheless, it is not entirely clear that they are absent inthe chimpanzee; Gannon, Kheck, Braun, & Holloway, 2005.)Furthermore, these areas were described to have “no sharpboundaries” with the temporal region (with areas 22 and 37,respectively; Brodmann, 1909). This suggests anatomical andfunctional continuity between posterior temporal areas andinferior parietal regions in humans, which is conWrmed by therecently observed connections between Wernicke’s regionand area 40 (Parker et al., 2005). Thus, we claim thatalthough the human phonological loop may include new cor-tical areas and connections, it derives from a preexistingauditory-inferior frontal circuit that is present in the non-human primate.

3. The phonological loop and mirror neurons

The working memory hypothesis has not been the onlyneurobiological proposal to explain early language evolu-tion. Based on the discovery of mirror neurons for grasping(which become active both when performing the action andwhen observing it) in a circuit involving the anterior intra-parietal area and area F5c of the monkey ventrolateral pre-frontal region, Rizzolatti and Arbib (1998), and later Arbiband Bota (2003) and Arbib (2005) developed anotherhypothesis for language origins. Considering the overlap ofthese networks with the homologues of language-speciWcregions, the potential role of these neurons in imitative pro-cesses (see also Miklósi, 1999; Rizzolatti & Arbib, 1999),and the fact that in monkeys, vocalizations have little vol-untary control, they claimed that the grasping mirror sys-tem provided the scaVolding for imitative behavior andvoluntary control over communication. They proposed asequence of events for language origins starting from animitation system for grasping, followed by the elaborationof complex gestural communication in which pantomimepermits to assign a primitive, conventionalized referencesystem to speciWc gestures. This mode of communicationdevelops into a conventionalized manual-based communi-cation system (protosign) that disambiguates the contentsof pantomime. Subsequently, the manual communicationsystem evolves into “protospeech,” which gives the vocalapparatus suYcient Xexibility, and eventually languageoriginates. In other words, the hand-based parieto-prefron-tal imitation system provided the behavioral plasticity nec-essary to generate a diversity of vocalizations which couldevolve into language. A related hypothesis has been put for-ward by Corballis (2003), who claims that there was an ini-tial stage in which communication was mainly vocal, thenbecame gestural and acquired symbolic characteristics, andWnally became vocal again. These hypotheses have beenpartly supported by the observation of a mirror system in

relation to sounds caused by actions (Kohler et al., 2002;see also Pizzamiglio et al., 2005), and in cells representinglip and mouth movements (Ferrari, Gallese, Rizzolatti, &Fogassi, 2003). The latter are especially important in thecontext of a recent report indicating that the macaque area44 is involved in orofacial motor responses, with only a fewneurons responding to combined manual and orofacialresponses (there was only one penetration site for combinedresponses out of eight sites with orofacial speciWcity; Pet-rides, Cadoret, & Mackey, 2005). Interestingly, chimpan-zees are able to match vocalizations to gesturing faces, thusvisually recognizing other vocalizing individuals and assess-ing their social situation (Izumi & Kojima, 2004). Althoughthis form of cross-modal capacity is considered to involvewidespread frontal, inferior parietal, and posterior tempo-ral regions (Calvert et al., 1999), it may also be related toassociations between orofacial mirror neurons and vocali-zation-sensitive neurons in the inferior frontal region.

Furthermore, a mirror system has been proposed to beinvolved in the generation of primitive concepts that serveas cognitive requisites for a lexicon of action-related utter-ances (Gallese, 2003), and evidence indicates that hand-ges-turing is related to conceptual learning (Goldin-Meadow &Wagner, 2005). There is also evidence of overlap betweenBroca’s area and the frontal representation of actions.Areas 44 and 45 have been observed to be active duringaction observation in humans (Rizzolatti & Craighero,2004), and a recent report in the monkey indicates that area45 is a region in which the integration of object and actioninformation occurs, which may have served as a prelinguis-tic link between verb and object (Nelissen et al., 2005). Arelated interpretation is that in humans, area 44 is moreinvolved in linguistic and non-linguistic communicationprocesses that are expressed in the control of variousaspects of the body, especially orofacial movements; whilearea 45 relates more closely to syntactic and semantic pro-cesses that are not directly expressed in motor control (Pet-rides, in press; Petrides et al., 2005; nevertheless, otherevidence points to a role of human area 44 in syntacticaland phonological working memory; Fiebach et al., 2005).

Other lines of evidence also support a close relationbetween hand control and communication ability. In pri-mates, there is a clear relation between handedness and lan-guage lateralization. Most apes tend to be right-handed,even for hand-signing (Hopkins & Leavens, 1998; Hopkinset al., 2005), and the perception of vocalizations is lateral-ized to the left hemisphere at least in monkeys (Hamilton &Vermeire, 1988). Aphasic patients and stutterers seem tobeneWt from pointing and from hand gestures (Hanlon,Brown, & Gerstmen, 1990; Mayberry, Jacques, & DeDe,1998), although it is not yet clear whether they do so simplybecause a manual system is the only one they have avail-able. Finally, pointing is a behavior that may originallyderive from a grasping action, has a clear communicativeintention, and appears in children before speech (Feyere-sien & Havard, 1999), which underlines the interdepen-dence between gestural and vocal communication.

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 45

The concepts of a mirror system and of the role of imita-tion in language origins are quite complementary to ourproposals (see also Arbib, 2005). We consider that gesturaland vocal communication coevolved to a large extent, andhave already put emphasis on the development of imitativeabilities in early language evolution (see Aboitiz & García,1997; Aboitiz, García, Brunetti, & Bosman, 2005; Bosman,García, & Aboitiz, 2004; Bosman, López, & Aboitiz, 2005).Nevertheless, we are somewhat cautious about the necessityto postulate a speciWc stage in which gestural, signing lan-guage was the main modality of symbolic communication,that preceded the origin of speech. In the next section, wewill discuss this issue in some detail.

4. Vocalizations and gestures in non-human primates

A Wrst question in relation to the hand-signing hypothesisis concerned with how relevant is signing versus vocaliza-tions in primates. Some authors claim that in wild non-human primates including chimpanzees, spontaneoushand-signing is more limited than vocal communication(Acardi, 2003; Seyfarth & Cheney, 2003), which is compati-ble with a continuity in vocal communication in humanevolution. Other studies have indicated that chimpanzeesand other apes engage in both gestural and vocal communi-cation, with vocal communication being more common inarboreal species (who have less visual contact) and ininstances in which there is no eye contact, and gesturalcommunication is more common in terrestrial species andin instances of social proximity (Pika, Liebal, Call, & Tom-asello, in press; Vogel, 1999; Hostetter, Cantero, & Hop-kins, 2001 for studies in captive chimpanzees).Furthermore, ape vocalizations tend to be highly ritualizedand related to evolutionarily urgent behaviors, such asdefense, food Wnding, and group traveling, while gesturesare performed in less stringent situations such as playing,and used quite Xexibly (Acardi, 2000; Liebal, Call, & Toma-sello, 2004; Pika et al., in press). There is evidence ofregional variability in the types of vocalizations emitted bywild chimpanzees, but this has been considered to dependon ecological factors and diVerences in body size ratherthan on social learning (Mitani, Hunley, & Murdoch, 1999).However, in populations of captive chimpanzees, groupdiVerences in vocalizations have been attributed to sociallearning since individuals within each group have diVerentorigins but nevertheless have little within-group variabilityand high intergroup variability (Marshall, Wrangham, &Acardi, 1999). Direct reference to objects or situations hasbeen hard to evidence, both in gestural or vocal communi-cation, but there is some evidence of referential gestures inrelation to food (Pika et al., in press), and of the use of gazealternation between the referred object (usually food) and ahuman experimenter (Leavens & Hopkins, 1998; Leavens,Hopkins, & Thomas, 2004). Although in vocal communica-tion there is even less evidence for referential communica-tion, it has been observed that bonobos (a variety ofchimpanzee) are able to produce acoustically distinct

screams during agonistic interactions, depending on therole they play in conXict (victim versus aggressor). Theauthors suggest that these scream variants are promisingcandidates for functioning as referential signals (Slocombe& Zuberbuhler, 2005). Summarizing, although there is bothvocal and gestural communication in non-human primates,in neither case they use symbols of the human kind (Pikaet al., in press). Thus, both modalities of communication areequally distant from human language. Although gesturalcommunication is more plastic, vocal communication hasin its favor that it uses the same sensorimotor circuit as spo-ken language (which is a strong argument for its evolution-ary continuity), and as will be discussed below, making thissystem more plastic would not be a diYcult evolutionarystep.

The fact that apes can be taught on sign language andnot on vocal communication has been claimed to supportthe notion that non-human primates lack the required vol-untary control over vocalizations. Therefore, speech mayhave not evolved without the aid of the hand-grasping sys-tem (Corballis, 2003). It seems that in this reasoning, a lim-ited capacity for ontogenetic learning is being used as anargument precluding the possibility of phylogenetic changetowards increasing plasticity and voluntary control. In ourview this makes little evolutionary sense. There is no a pri-ori reason why a selective trend could not have originatedtowards increasing plasticity and control of the vocal tract,leading to the same or even more behavioral Xexibility(including combinatorial abilities) than that observed inhand coordination. Vocal imitation and plasticity has beenobserved in species such as elephants, seals, and dolphins(Janik, 2000; Poole, Tyack, Stoeger-Horwath, & Watwood,2005; Shapiro, Slater, & Janik, 2004), suggesting that ahand-grasping system is not a prerequisite for the acquisi-tion of voluntary control of the vocal system and imitativecapacity (elephants have a grasping trunk, but what aboutseals and dolphins?). More generally, in animals, mirrorneurons and the ability to recognize and imitate actionsmay not be restricted to the hand-grasping system (Bosmanet al., 2004; Miklósi, 1999). Thus, we concur with Rizzolattiand Arbib (1999) in that “the F5 ‘mirror’ mechanism repre-sents a particular variant of an ancient mechanism thatunderlies a variety of behaviors” (p.152).

5. The neural substrates

Let us examine more closely the neuroanatomical andneurophysiological control of the vocal apparatus. Arbiband Bota (2003) assert that in non-human primates, thecortical control of vocalizations is strongly dependent onthe anterior cingulate, while the homologue of humanBroca’s area is proposed to be related to hand control, withits extensive connections with the inferior parietal lobe.First, we would like to point that cingulate control forvocalizations is found in monkeys and humans, and in bothcases its function has to do with motivation rather thanprocessing (Aboitiz et al., 2005; Paus, 2001). A second issue

46 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

relates to the proposed role of the inferior parietal lobe inboth hand control and human linguistic processes (Rizzol-atti & Arbib, 1998). We already mentioned that the inferiorparietal regions (including area 40) of the human are prob-ably more complex than the monkey inferior parietal andintraparietal areas (Castiello, 2005). Furthermore, inhumans, the functions of hand control and linguistic pro-cessing could be segregated in the inferior parietal lobe.Patients with circumscribed lesions of areas 39 and 40 showsevere deWcits for imitation of meaningless gestures (Gold-enberg, 1997; Goldenberg & Hagmann, 1997). An imagingstudy indicated area 40 and parietal area MT/V5 in imita-tion of hand postures (Goldenberg, 2001), althoughanother report found activation only in area MT/V5 (Peig-neux et al., 2000). A more recent analysis of visually guidedgrasping detected activity in the anterior intraparietal sul-cus, involving mostly the dorsal aspect of area 40 (Frey,Vinton, Norlund, & Grafton, 2005; see also Castiello, 2005).On the other hand, the phonological storage functioninvolves mainly the more ventral supramarginal gyrus(Smith & Jonides, 1998).

The third issue in this context relates to the role of theinferior frontal areas in hand grasping and language pro-cessing. As mentioned, there is human evidence suggestingthat the representation of these functions overlaps in thisregion (Rizzolatti & Craighero, 2004). In the monkey, area45 has been shown to participate in the recognition of handgrasping (Nelissen et al., 2005), but the study by Petrideset al. (2005) indicates that area 44 is almost devoid of hand-grasping neurons but rather contains orofacial motor neu-rons. More importantly, exponents of the hand-signinghypothesis have underlined the presumed absence of volun-tary, prefrontal control over vocalizations in monkeys,which would suggest that these areas are mainly related tohand control (Arbib & Bota, 2003; Corballis, 2003). How-ever, as we mentioned above, the ventrolateral prefrontalcortex of monkeys contains a vocalization-sensitive domain(Romanski & Goldman-Rakic, 2002; Romanski et al.,2005) and a motor representation of the larynx (Jürgens,2003). Electrical stimulation of the latter can elicit vocalfold movements (Hast, Fischer, Wetzel, & Thompson,1974), and cortical lesions in the supplementary motor areacan signiWcantly reduce the total number of vocalizationsemitted by monkeys (Gemba, Miki, & Sasaki, 1997; Kirzin-ger & Jürgens, 1982), indicating a degree of prefrontal con-trol over the vocal apparatus. Previously, we suggested thatthe prefrontal, vocalization-sensitive neurons describedabove represent the phylogenetic precursors of a vocaliza-tion mirror system (Bosman et al., 2004). All that is neededis that these neurons participate in articulatory processes,which would not be a diYcult evolutionary step. An elabo-ration of this auditory-vocalization circuit may have beensuYcient to develop imitative vocal behavior, leading to anincipient phonological loop. In humans, a fronto-parietal-temporal network that responds both to perception andoral production of sounds including speech and tonal pro-duction has been identiWed (Hickok et al., 2003), and a

recent fMRI study has demonstrated that listening tospeech activates a superior portion of the ventral premotorcortex that largely overlaps with a speech productionmotor area (Wilson, Saygin, Sereno, & Iacoboni, 2004).This evidence is consistent with the existence of a humanvocalization mirror system, partly derived from the vocali-zation-sensitive regions above described in the monkeyfrontal cortex. In this context, another organ that is essen-tial for human speech is the tongue. Interestingly, there is aphylogenetic trend towards the strengthening of cortico-hypoglossal projections (involved in tongue control) fromnon-primate mammals via non-human primates to humans(Jürgens & Alipour, 2002), which is consistent with theindependent development of cortical control over thevocalization apparatus in the human lineage. The tongue isused in other functions such as swallowing, but these main-tain their reXex nature and are presumably conservedamong primates. Speech is perhaps the function that mostbeneWts from a movable and voluntarily controlled tongue.

6. Why developing a plastic vocalization system?

The exquisitely Wne-tuned movements that characterizespeech production require a delicate control of the vocalapparatus and of the lips, tongue, jaw, and larynx (Dron-kers & Ogar, 2004). In humans, motor control over this sys-tem is partly located in the precentral gyrus of the insula(Dronkers, 1996) and in the inferior frontal gyrus (Hilliset al., 2004). If as mentioned, primate vocalizations are usedin evolutionarily “urgent” functions (Pika et al., in press), itis reasonable to consider that in hominid evolution theysuVered a higher selective pressure than gestures. In somecircumstances, increasing vocal plasticity and cortical con-trol over the phonatory apparatus may have been selectivebeneWt, as they allowed to convey more detailed informa-tion about evolutionarily urgent issues. One possibility isthat prosodic and gestural markings permitted a strongermother-and-child relation, and other kinds of social bond-ing that enhanced group cohesiveness and cooperation(Kuhl, 2003; Falk, 2004). More speciWcally, early homininmothers engaged in reciprocal vocal (and gestural) interac-tions with their progeny (infants or children). In this way,both became “locked” in a mutual dynamics where thechild gradually generated a template of his/her mother’sgestures and vocalizations that permitted the maintenanceof mutual communicative interactions, largely conveyingemotional information (Aboitiz & Schröter, 2004). In thesecircumstances, there was a selective prize for those individ-uals with an increased vocal motor control, and eventually,with an increased memory span to remember complexsequences of utterances in order to facilitate recognitionand maintain the reciprocity in social interactions (this doesnot exclude the parallel development of gestural communi-cation). In this line, the evolution and development of bird-song provides a useful model for early phonologicalacquisition. Birds able to learn and transmit more complexsongs have a selective beneWt over those who develop less

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 47

elaborate sequences (Gil-da-Costa et al., 2004; Doupe &Kuhl, 1999; Okanoya, 2004; Jarvis, 2004; see also Kuhl,2003 for the social signiWcance of early language).

The plasticity of the vocalization apparatus posed it as agood candidate to communicate referential associationsthat became conventionalized in the community. Thus,complex vocalizations may have been related Wrst to highlyemotional situations, and were accompanied by gesturesincluding facial movements and ritualized pantomine.These complex, multimodal communication signals becameassociated to speciWc events, generating the most basicforms of conventionalized reference. Eventually, and withthe further evolution of the phonological capacity, thesemultimodal signals became dominated by vocalizations,but never (not even in present-day human communication)entirely lost their multimodal, gestural-vocal nature.

A Wnal issue relates to imitative abilities. In macaques,there is evidence for cognitive imitation (Subiaul, Cantlon,Holloway, & Terrace, 2004), and natural imitation isstrongly facilitated by joint attention (Kumashiro et al.,2003). In another study, it was found that neonatal chim-panzees were able to recognize and imitate human facialgestures, but this ability is lost after 2 months of age; onthe other hand, in humans imitation gestures appear atapproximately 8–12 months (Myowa-Yamakoshi, Tomo-naga, Tanaka, & Matsuzawa, 2004). This evidence sug-gests that the capacity to imitate is either ancient or hasappeared more than once in primate evolution, and is nota uniquely human characteristic. However, all these stud-ies have been performed in controlled laboratory condi-tions. Another issue is whether chimpanzees and otherprimates imitate in natural conditions. There has beenmuch controversy as to whether apes are able to transmitbehavioral patterns by imitation or by processes like ritu-alization, in which stereotyped behaviors are used toanticipate to initiate play or mating with another individ-ual (for review see Vogel, 1999). Some evidence suggeststhat in apes, ritualization is a major element in sociallytransmitted behavior (Pika et al., in press), and severalgestural behaviors including pointing and some forms ofpantomime may be conceived as originating in this man-ner. Nevertheless, other evidence indicates that chimpan-zees and other apes are also able to learn by socialimitation. Recently, Whiten, Horner, and de Waal (2005)trained some captive chimpanzees in one of two tech-niques to obtain food from a box. Subsequently, theseindividuals transmitted this behavior to the other mem-bers of the community. Furthermore, animals that hadlearn one technique but the majority in their group hadlearned the other, eventually changed to the majoritybehavior. The emerging picture is that apes are able ofimitation, but within a repertoire of several social learningmechanisms, and in a much more limited form thanhumans (Whiten, 2005). Thus, we agree with Arbib (2005)in that these forms of imitation are diVerent from the com-plex imitation capacity involved in pantomime and other,human forms of imitation, but consider that these provide

a starting point for the development of more complex imi-tative capacities, leading to more elaborate forms of com-munication.

After all this discussion, we consider that parsimonyindicates that the most likely situation is that both, gesturaland vocal communication coevolved intimately, as they stilldo now, but we see no grounds or evidence supporting thepresumed ancestral, symbolic signing stage (Aboitiz et al.,in press; Bosman et al., 2004; and in press). In this sense,our position is somewhat close to Arbib’s (2005), who sug-gests an “expanding spiral” in which gestural communica-tion including complex pantomime coevolved with vocalcommunication, each potentiating the development of theother. It diVers, however, from Corballis’ (2003) position,proposing a speciWc stage in which symbolic communica-tion was predominantly hand-gestural, which was eventu-ally “taken over” by vocal communication. SpeciWcally, weconsider unlikely that such a stage became an evolution-arily stable condition, able to diversify and propagate.Hands are used for other behaviors such as tool use andcarrying objects, and do not appear as optimal communica-tion devices as long as they require that individuals stay infront of each other doing nothing else with their hands. So,this modality might work in idle situations but not so muchin circumstances of behavioral coordination. Furthermore,there is no evidence that gestural communication was evermore developed than it is now in spoken languages, lackingseveral of the crucially deWning characteristics of language(note that human sign languages are usually derived from,or arise within the context of a vocal-communicating com-munity). Thus, even if voluntary control was initially moredeveloped for hand control than for vocal communication,the most likely interpretation is that gestural communica-tion never reached a symbolic stage without the aid of anelaborate vocal communication system.

7. Syntax: Memory and recursion

Phonology is not the only linguistic function that makesuse of short-term memory. Lexical processing, in which thephonological representation of a word becomes associatedwith a meaning, also implies the transient coactivation of therespective mnemonic representations. Abundant evidencesuggests that lexical memories consist of activated associativenetworks involving say, object- or motor-speciWc regions (inthe cases of names for objects and action words, respec-tively), with language-speciWc regions (Damasio & Tranel,1993; Damasio, Grabowski, Tranel, Hichwa, & Damasio,1996; Pulvermüller, 1999, 2005; Pulvermüller, Lutzenberger,& Preissl, 1999; see also Fuster, 1995a, 1995b, 2003). Never-theless, and in accordance with the concept of associativememory, naming networks are not likely to be rigid modulesor hardwired centers; they should rather be conceived ashighly modiWable by experience (Damasio et al., 1996; Fus-ter, 1995a, 2003). This evidence conWrms Geschwind’s (1965)early proposal that the human brain was unique in its abilityto perform cross-modal cortical associations, ant that this

48 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

enabled it to the development of a naming system. Thiscapacity is related with the development of posterior tempo-ral lobe and inferior parietal areas, which show great individ-ual variability in their morphology and have been alsorelated to the generation of the phonological loop (Ide, Rod-ríguez, Zaidel, & Aboitiz, 1996; Ide et al., 1999).

Furthermore, the processing of more complex linguisticitems, such as syntactical structures, is also strongly depen-dent on short-term memory. As Fuster (1995a) puts it,“ƒlanguage, especially when it is new, complex, andextended in time, makes constant use of those functions ofmemory and set. As I speak, I need to keep track of what Ijust said a few moments ago and, at the same time, preparefor saying what is in accord with that. The predicate isdependent on the subject, the verb on the subject and thepredicate, the dependent clause on the larger sentence, andso on. All these are, in essence, cross-temporal contingen-cies, and in speech there is a running reconciliation of thesecontingencies that constantly change, interleaved andembedded within another. It is the dorsolateral prefrontalcortex that normally eVects that reconciling, with its graspof the short-term past and the short-term future” (pp. 280–281; see also Fig. 2). This comment, although stronglyappealing, is perhaps too coarse-grained for the purposes ofthis paper. In the following sections, we will intend to dis-sect some of the complex linkages that exist in diVerentmemory domains during language processing.

According to Pinker and JackendoV (2005), syntax con-sists of the principles by which words and morphemes areconcatenated into sentences, helping to determine how themeanings of words are combined into the meanings ofphrases and sentences. Syntax consists of several elements,one of which is word order, in which the distinct elementsare conventionally arranged in a speciWc order in each lan-guage; another component is agreement, marking inXec-tions in verbs or adjectives for number, person, gender, andother features of related nouns; and yet another is case-marking (nominative, accusative, and others). A fourthcomponent of syntax consists of the hierarchical construc-tion of phrases, in which each phrase corresponds to a spe-ciWc constituent of meaning. Furthermore, one

fundamental property of this hierarchical arrangement isits recursivity. Generally speaking, recursion consists of theapplication of some function onto itself (phrases may becomposed of nested phrases), which permits to iterate thisfunction endlessly, thus generating diVerent hierarchicallevels according to the iteration sequence, and permittingthe manipulation (movement) of the elements in this hierar-chy (Chomsky, 1991; Hauser et al., 2002; see also Fitch &Hauser, 2004). An important element in the generation ofrecursive structures is the so-called long-distance dependen-cies between words, which bracket phrases embeddedwithin larger phrases (Chomsky, 1991). Thus, embeddedphrases can be moved to diVerent positions within a sen-tence, changing the canonical order of the original phraseto transform it into say, a passive sentence or a wh-ques-tion. Moved phrases can be tracked to their original posi-tions by a “trace” that connects the new position with theextraction site. Some authors in the chomskyan traditionclaim that recursivity is the most fundamental property ofhuman language, is modularly separate from other cogni-tive functions, and is highly unlikely to result from theprocess of natural selection. This ability is claimed to benon-existent in primates, as tamarin monkeys were shownnot to be able to learn a quite simple recursive language,consisting of n instances of a symbol A followed by ninstances of symbol B (Fitch & Hauser, 2004). Nevertheless,Pinker and JackendoV (2005) reply that it is not clear thatthis symbol sequence represents a truly linguistic structure,as no known language shows this kind of recursivity. Aswill be discussed below, we consider that the capacity forlinguistic recursion originated in the context of an expand-ing working memory capacity that permitted to manipulatethe diVerent items composing a complex sequence of words(or phrases). In primates, this capacity is highly limited dueto the relatively poor development of cortico-cortical asso-ciations compared to humans, but with increasing brainsize and subsequent cultural evolution, these networksbecame robust enough to manipulate more complex items.

Our proposal is that recursivity and movement of phrasecomponents can only exist if backed by a strong short-termmemory mechanism that allows one to keep track of the

Fig. 2. Highly schematic concept of cortical interactions between networks of posterior and frontal cortices in the construction of a simple phrase. Thisimplies the coactivation of several short-term memory networks, each representing a phonological representation (squares) and a lexical representation(circles), which although are activated in sequence, they need to be maintained in memory and associated as the phrase is being processed. Once the mean-ing of the phrase has been extracted, it is bound or integrated as a semantic “chunk” that can be mentally manipulated in the context of a larger sentence(Gibson, 1998; Hagoort, 2005). In this context, it is of interest to mention Glassman’s (2003) conception of two phenomenal levels during working memoryoperation, binding together of many attribute representations within each respective memory “chunk,” and then the combinatorial play among three orfour distinct chunk representations. Anatomical details are not intended to be speciWc. The Wgure is a modiWcation and composite of Fuster’s (2003)Fig. 7.9 and Pulvermüller’s (2005) Fig. 1.

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 49

long-distance dependencies present in both embeddedphrases and syntactic movement (see also Pinker, 1995).Short sentence processing imposes a rather small load onworking memory capacity, and does not require a special-ized or too elaborate short-term memory network. Process-ing simple but relatively long, canonical sentences, in whichhead-dependent relations have to be maintained for sometime until the phrase ends being processed, impose an addi-tional load on memory and require relatively more robustnetworks. Finally, transformational movement imposes evenhigher memory loads, thus requiring the activation of morecomplex networks. In human evolution, those individualsable to develop more robust short-term neuronal networkswere able to mentally manipulate the components of a sen-tence, thus communicating more complex messages, andselecting what to communicate in diVerent circumstances.This permitted them to cooperate better and to establishstronger social bonds. An “expanding spiral” developedbetween increased working memory capacity and morecomplex communication, resulting in the evolution of rela-tively intricate recursive abilities. Nevertheless, it is necessaryto note that perhaps not all syntactically ordered languageshave the properties of recursion claimed by Hauser et al.(2002). The amazonian language Piraha has been claimed tolack any evidence of recursion (Everett, 2004; see also Pinker& JackendoV, 2005) but has a clear phonology, morphology,syntax, and sentence organization. It is not clear if this lan-guage never had recursion or lost it, but in the case that thisWnding is conWrmed, it would indicate that syntactic lan-guages may exist in which there are no recursion rules. Thus,it is conceivable that modes of communication with primi-tive syntactic rules, not including recursion (in the sense ofphrase movement properties), but being speciWc on otherattributes such as word order and agreement, preexisted tomore complex languages. With the involvement of increas-ing working memory resources, these languages tended toevolve toward more complex, recursive grammars.

8. Models and experimental studies on working memory and syntactical movement

In the past, short-term memory was seen by some scholarsto be a mere constraint that puts limits to syntactic process-ing (Miller & Chomsky, 1963), while more recent authorsconsider that it has a much more active role in parsing (Gib-son, 1998; Just & Carpenter, 1992; King & Just, 1991; King &Kutas, 1995; see also Müller & Basho, 2004). In fact, it hasbeen proposed that short-term memory mechanisms make itpossible to maintain distinct linguistic elements on line whilea larger structure is being processed (Gibson, 1998, 2000; Just& Carpenter, 1992). In these views, syntactical parsinginvolves two kinds of processes: integration and short-termmemory. Integration refers to the cost of integrating distanthead-dependent relations in a phrase, which may neuro-physiologically relate to a “binding” mechanism that gluesperceptual (lexical) elements into a coherent frame (Hagoort,2003, 2005; Schoenemann, 1999; see Fig. 2). Interestingly,

beside language, Broca’s area has been also involved in musi-cal processing, and the integrative mechanisms involved havebeen proposed to be similar to those for syntactic parsing(Patel, 2003; Patel, Gibson, Ratner, Besson, & Holcomb,1998; although some argue that they are perhaps not so simi-lar to the linkage of phonology to the lexicon or the way inwhich syntax supports a compositional semantics). Gibson(1998) also claims that there are memory costs associatedwith the resources required to store the incomplete currentinput string as it is being processed, in order to appropriatelyassign thematic roles onto syntactic constituents. Gibsonhypothesizes that each element that does not yet have a the-matic role (such as “agent,” “patient,” etc.) while the sen-tence is being processed imposes a burden on workingmemory. As we have discussed above, the neural networksinvolved in these processes include language-related areas(especially Broca’s area and its vicinities), but are also highlywidespread by virtue of the associative nature of these mem-ories. In this line, intracranial recording studies have revealedthat neurons that participate (but are not necessarily essen-tial) in verbal short-term memory are widely spread in bothhemispheres (Ojemann, SchoenWeld-McNeill, & Corina,2002). Furthermore, individual neurons usually relate to onlyone mnemonic function and are surrounded by nearby neu-rons having diVerent relationships, which suggests the exis-tence of interlacing networks, especially well suited forassociative interactions (Ojemann, 2003).

Interestingly, Broca’s aphasics seem to have a speciWcimpairment in tracking the traces that connect componentswith their extraction sites during syntactical movement(Grodzinsky, 2000). Some authors claim that the inabilityof Broca’s aphasics to track traces may reXect a workingmemory deWcit (for example, Hickok, 2000; Müller, 2000;Stowe, 2000; Szelag & Pöppel, 2000). Furthermore, recentimaging analyses have shown that diVerent forms of syntac-tic movement speciWcally activate the same cortical regions:the left inferior frontal gyrus and bilaterally, the posteriorsuperior temporal cortex (Ben-Shachar, Hendler, Kahn,Ben-Bashat, & Grodzinsky, 2003; Ben-Shachar, Palti, &Grodzinsky, 2004), which is anatomically consistent withthe activation of an auditory short-term memory circuit(Gottlieb et al., 1989; Pasternak & Greenlee, 2005; Roman-ski, Bates, et al., 1999; Romanski, Tian, et al., 1999). Otherfunctions, regulating intra-sentential dependencies that arediVerent from syntactic movement, seem to be related toactivation of other regions such as the anterior insula, ven-tral precentral sulcus, and the superior frontal gyrus (Grod-zinsky, in press). Much recent evidence indicates thatBroca’s area is speciWcally activated with syntactic move-ment and during processing of long-distance dependencies,which are considered to imply working memory costs(Caplan & Waters, 1999; Caplan et al., 1998, 2000; Cookeet al., 2002; Fiebach et al., 2002; Friederici, 2004; Kaan &Swaab, 2002; King & Kutas, 1995; Stromswold, Caplan,Alpert, & Rauch, 1996). For example, in an fMRI study,Cooke et al. (2002) report that the left inferior frontal cor-tex is recruited to support the cognitive resources required

50 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

to maintain long-distance syntactic dependencies duringthe comprehension of complex grammatical sentences. Fie-bach et al. (2002) were able to dissociate memory and inte-gration costs by using subject-initial and object-initial, longand short wh-questions. Object-initial sentences werehighly dependent upon the subject that would be encoun-tered later, while subject-initial sentences do not depend ofthe later appearance of an object argument. Thus, long,object-initial sentences required a higher memory load butthe same integration costs as long, subject initial sentences.In these conditions, the authors reported a sustained nega-tivity over the left frontal scalp that was maximal for longobject wh-questions. In a subsequent study, the sameauthors found that Broca’s area (particularly area 44) wasespecially activated when processing complexly embeddedsentences, in comparison with similar grammatical struc-tures which put less load on working memory (Fiebachet al., 2005). These authors conclude that this evidencestrongly supports the role of Broca’s area in syntacticalworking memory processes.

Summarizing, evidence suggests that short-term memorymechanisms do more than putting limits to syntactical pro-cessing; they rather play an important role in this phenome-non. Furthermore, we concur with Fuster (1995a, 1995b)and others in that the kind of memory involved in syntacti-cal processing is based on the transient activation of associa-tive networks in the cerebral cortex, and is in principle notdiVerent than other forms of cortical memory, whose precur-sors can be found in the monkey brain. Admittedly, we arenot claiming that language and syntax can be fully explainedby memory mechanisms. There are many elements of pho-nological, lexical, and syntactical processing such as the met-rical structure of words, inXectional rules, recognition ofsyntactic components and other phenomena that may wellbe language-speciWc, and are not easily explained by mem-ory mechanisms or by current cognitive theories (Pinker &JackendoV, 2005). Language is clearly a complex adaptationinvolving specializations in perception, production, and pro-cessing at several levels. Other cognitive phenomena, such asthe ability to recognize actions, categorizing, or problem-solving, are strongly implicated as well and may have servedas prerequisites for linguistic evolution (Fadiga & Craighero,2004; Gallese, 2003; Langacker, 1987, 2000; Mandler, 2004;Nelissen et al., 2005). Nevertheless, we mentioned above thatactive memory is deWned in the context of near-futurebehavior, i.e., implies manipulation of cognitive items toattain a Wnal goal. In a similar way, it permits to manipulatethe distinct components of a sentence in diVerent ways inorder to extract meaning. Thus, processes such as categoriza-tion and problem-solving, although not identical to workingmemory mechanisms, are also highly dependent on the on-line maintenance of information.

9. Modularity or associative networks for working memory?

In the context of this discussion, there have been recentcontroversies about the modular nature of the memory

mechanisms involved in syntactical processing. Someauthors contend that the system for syntactical processingis separate from the phonological, lexical or semanticdomains (Caplan, 1987; Caplan & Waters, 1999; Ferreira &Clifton, 1986; Martin & SaVran, 1997; Martin, 1987), whileothers consider that grammar is intrinsically linked to them(Langacker, 2000; Lieberman, 2002). In our view, the verbalworking memory system is not a single indissociable ele-ment, but on the other hand each component (phonologi-cal, lexical, and syntactic) is not independent but highlyinteracting with the others. This is to be expected if activememories are essentially associative (Fuster, 1995a). Thus,there are diVerent but partially overlapping network sys-tems related to each domain involved in language process-ing, which is consistent with neurobiological evidence(Fuster, 1995a, 2003; King & Kutas, 1995; Levy & Gold-man-Rakic, 2000; Pasternak & Greenlee, 2005; Romanski,Tian, et al., 1999). This view agrees with fMRI results iden-tifying three relatively separate regions of functional spe-cialization in the inferior frontal gyrus: phonology, syntax,and semantics (for review, see Bookheimer, 2002). There-fore, lexical networks are diVerent but overlap in importantaspects with other kinds of networks involved in phonolog-ical and in syntactical processing, which explains why insome instances increasing syntactic load interferes withphonological working memory and vice versa (Just & Car-penter, 1992). In fact, we consider that it is precisely theoverlap between these networks that allows to process sen-tences as integrated phonological, lexical, and syntactic uni-ties from which a single meaning can be extracted. Puttingit another way, syntactical working memory needs to be‘anchored’ in lexical working memory networks in order toidentify the words, their meaning, and their grammaticalproperties, while lexical working memory needs to be‘anchored’ in phonological representations that contain theacoustic and motor dimensions of the diVerent words. Inthe words of Lieberman (2002), “verbal working memoryappears to be an integral component, perhaps the key com-ponent, of the human functional language system, couplingspeech perception, production, semantics, and syntax” (p.70). Again, the integration of these diVerent processing lev-els may be conceived as a “binding problem” in which theactivities associated to each mechanism become coordi-nated and interdependent (Hagoort, 2005; Singer, 2001).This view is thus in an intermediate position between thosewho consider a separate neural subsystem for each process-ing domain (Caplan, 1987) and cognitive approaches thatconsider grammar and meaning as inseparable componentsof language (Langacker, 2000).

10. Discussion

In this article, we have updated some of our previousproposals (Aboitiz, 1995; Aboitiz & García, 1997) in whichwe proposed that the language regions arose as a specializa-tion of auditory-vocal working memory networks which ina Wrst instance elaborated into a primitive phonological

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 51

loop. Eventually, this apparatus recruited additional mem-ory networks representing meaning, contributing to thedevelopment of increasingly complex forms of social com-munication. The expansion of this system allowed the man-agement of complex utterances in speciWc orderings such asto convey more detailed meanings and to avoid ambiguityin communication. The brain regions supporting languageare known to be more extense than the relatively narrowcircuits that we have pointed in this article (Dronkers &Ogar, 2004; Dronkers et al., 1992; Kaan & Swaab, 2002),and a more complete discussion of primate–human homo-logues would, ideally, include these areas too. However, atthis point this would be a too ambitious project and wehave preferred to restrict our analysis to the regions thathave been classically involved with language processing.

The networks involved in syntactical processing are con-ceived to be more extended than the phonological loop (asthey need to maintain online items more complex than justphonological representations), but the evidence discussedsuggests that they are still partly restricted to the language-speciWc regions (especially in the frontal lobe). Our hypoth-esis is that in the non-human primate, there are muchsimpler but comparable networks, which have not acquiredthe robustness necessary to maintain and manipulate thecomplex information items required for syntactical- andeven less for recursive sentence processing. In other words,we claim that the issue of the appearance of some syntacti-cal rules, including the recursive properties in language pro-cessing, were behavioral innovations that became possibledue to the elaboration on preexisting neural networks,whose function was (and is) to maintain items online dur-ing the execution of a speciWc behavior. In order to developthese more stable and robust networks, a conversationalability must have existed in which individuals were able toengage in reciprocal phonological (and meaningful) inter-actions for suYcient time, to permit the maintenance of a“state of mind” that captured attentional and memoryresources. Cultural evolution may have provided a meansfor increasing the complexity of these networks. The mod-ern human brain had already acquired its actual size about195,000 years ago (MacDougall, Brown, & Fleagle, 2005),long before there were any signs of cultural activity indicat-ing complex symbolic thinking, which date from about75,000 years ago (Henshilwood, d’Errico, Vanhaeren, vanNiekerk, & Jacobs, 2004). This suggests that increasingbrain size was not suYcient for a fully developed language,and that further cultural evolution was essential for lan-guage acquisition. The developing cerebral cortex is capa-ble of incredible plastic rearrangements in response toenvironmental (and social) stimuli (Krubitzer & Kahn,2003). Thus, cultural selection of behaviors includingincreasingly more sophisticated social interactions, toolmanipulation, and other elaborate conducts may haveprovided the means to develop increasingly elaborateshort-term memory network systems, linking phonology,meaning, and syntax (Aboitiz, 1988). On this point, we mayagree with Arbib (2005), who makes the explicit claim that

human brain size evolution was not driven by the need forsyntax, but only by the demands of protolanguage, withsyntax being the fruit of cultural evolution. Nevertheless,this does not exclude the possibility of continuing geneticselection for the development of highly tuned sensorimotorcircuits, which permitted better cortical control and moreeYcient memory networks within the context of a Wxedbrain size (Aboitiz, 1988, 1995). Finally, there is recent evi-dence in humans of rapid adaptive evolution of at least twogenes controlling brain size, which suggests that geneticevolution of the human brain is still an undergoing process(Evans et al., 2005; Mekel-Bobrov et al., 2005).

The present perspective has been discussed in the contextof two current hypotheses on language evolution. The Wrstcomes from students of mirror neurons for grasping, whoclaim that a mirror system was essential for the evolution ofa brain that could support language. As mentioned, weagree that a mirror system may have been especially impor-tant for recognizing actions and for the development of imi-tative capacities, which in turn were essential for thedevelopment of a phonological loop and other cognitive andlinguistic capacities. We are more wary on the assumptionthat there was an initial, symbolic hand-signing stage priorto the origin of speech. We consider that this presumed stageis not yet backed by suYcient evidence and there are simpleralternatives, such as the acquisition of a vocalization mirrorsystem in early hominids within the context of a multimodalvocal–gestural communication system. In this sense, therecent Wnding by Petrides et al. (2005) of orofacial neuronsin the macaque’s area 44 may point to a brain location inwhich associations between speciWc vocalizations and facialgestures are performed. Furthermore, even in the case thathand-signing served as an initial scaVolding for the develop-ment of vocal linguistic abilities, the subsequent evolution ofthe language areas was in our view, highly dependent of thedevelopment of auditory-vocal short-term memory net-works that are present in non-human primates. The secondperspective relates to the generativist approach whose expo-nents, in their latest writings, have proposed that the capac-ity for recursion is unique to human language (which mightbe correct), and is unlikely to have originated by naturalselection since it is a single characteristic, not arising as theresult of sequential steps (Hauser et al., 2002; this perspec-tive has been contested by Pinker & JackendoV, 2005; andsee reply by Fitch, Hauser, & Chomsky, 2005). In our view,whether the behavioral phenomenon of recursion is indeedunique to human language, and whether there are simplerand more complex (derived) forms of recursion in diVerentlanguages remain as empirical questions. However, we alsoconsider that the acquisition of recursion has been only pos-sible through the increasing complexity of the short-termmemory networks involved in meaningful communication,which most likely has been a gradual process (via either cul-tural or genetic evolution).

There have been other neurobiological theories of earlyspeech evolution, and we will mention only a few of them.The motor theory of speech perception claims that the

52 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

listener processes speech by comparing the input with amotor template for speech production (Liberman & Mat-tingly, 1985). Another proposal is the concept of categori-cal perception, where speech sounds are not directlytranslated into their acoustical parameters but rather arelabeled within distinct phonological categories (Kuhl,1992). These two theories are entirely consistent with theexistence and evolution of a phonological loop (see Lie-berman, 2002). Finally, there is the concept of selectionfor precise motor timing which permitted the complexarticulation of speech movements (Dronkers & Ogar,2004), which were related with the acquisition of otherWne motor tasks such as object manipulation and stonethrowing (Calvin, 1983). Again, this idea is complemen-tary to our proposals, although as said we are not surethat control of hand coordination was a strict requisitefor the evolution of vocal communication. Rather, thetwo evolved together, in an intimate relationship.

Finally, although relying on relatively few geneticchanges (Culotta, 2005), language and human communi-cation involve modiWcations at several functional levels,including gross morphology, motor control, perceptualmechanisms, and the elaboration of speciWc neural net-works participating in higher aspects of phonological, lex-ical, and semantic processing. Our emphasis in this articlehas been to point to neural structures and networks thatparticipate in certain aspects of language processing, andtracking these to more simple networks in the primatebrain, which have a similar topographic organization asin the human and participate in similar processes. Weconsider that this evidence makes a case for evolutionarycontinuity (homology) between the respective neural sys-tems.

Acknowledgment

This work was supported by the Millennium Nucleus forIntegrative Neuroscience.

References

Aboitiz, F. (1988). Epigenesis and the evolution of the human brain. Medi-cal Hypotheses, 25, 55–59.

Aboitiz, F. (1995). Working memory networks and the origin of languageareas in the human brain. Medical Hypotheses, 44, 504–506.

Aboitiz, F., & García, R. (1997). The evolutionary origin of the languageareas in the human brain. A neuroanatomical perspective. BrainResearch Reviews, 25, 381–396.

Aboitiz, F., García, R., Brunetti, E., & Bosman, C. (in press). The origin ofBroca’s area and its connections from an ancestral working/activememory network. In K. Amunts & Y. Grodzinsky (Eds.), Broca’s area.Oxford: Oxford University Press.

Aboitiz, F., García, R., Brunetti, E., & Bosman, C. (2005). Imitation andmemory in language origins. Neural Networks, 18, 1357.

Aboitiz, F., & Schröter, C. (2004). Prelinguistic evolution and motherese:A hypothesis on the neural substrates. Behavioral and Brain Sciences,27, 503–504.

Acardi, A. C. (2000). Vocal responsiveness in male wild chimpanzees:Implications for the evolution of language. Journal of Human Evolu-tion, 39, 205–223.

Acardi, A. C. (2003). Is gestural communication more sophisticated thanvocal communication in wild chimpanzees? Behavioral and Brain Sci-ences, 26, 210–211.

Arbib, M. (2005). From monkey-like action recognition to human lan-guage. An evolutionary framework for neurolinguistics. Behavioral andBrain Sciences, 28, 105–167.

Arbib, M., & Bota, M. (2003). Language evolution: Neural homologiesand neuroinformatics. Neural Networks, 16, 1237–1260.

Awh, E., Smith, E. E., & Jonides, J. (1995). Human rehearsal processes andthe frontal lobes: PET evidence. Annals of the New York Academy ofSciences, 769, 97–118.

Baddeley, A. (1992). Working memory. Science, 255, 556–559.Baddeley, A. (2000). The episodic buVer: A new component of working

memory? Trends in Cognitive Sciences, 4, 417–423.Baddeley, A. (2003). Working memory: Looking back and lookin forward.

Nature Reviews Neuroscience, 4, 829–839.Baddeley, A. D., & Hitch, G. J. (1974). Working memory. In G. A. Bower

(Ed.), The psychology of learning and motivation. New York: AcademicPress.

Baddeley, A. D., Papagno, C., & Vallar, G. (1988). When long-term learn-ing depends on short-term memory. Journal of Memory and Language,27, 586–595.

Barbas, H., & Pandya, D. N. (1989). Architecture and intrinsic connectionsof the prefrontal cortex in the rhesus monkey. Journal of ComparativeNeurology, 286, 353–375.

Belin, P., & Zatorre, R. J. (2000). ‘What,’ ‘where’ and ‘how’ in auditorycortex. Nature Neuroscience, 3, 965–966.

Ben-Shachar, M., Hendler, T., Kahn, I., Ben-Bashat, D., & Grodzinsky, Y.(2003). The neural reality of syntactic transformations—Evidence fromfMRI. Psychological Science, 14, 433–440.

Ben-Shachar, M., Palti, D., & Grodzinsky, Y. (2004). Neural correlates ofsyntactic movement: Converging evidence from two fMRI experi-ments. Neuroimage, 21, 1320–1336.

Bookheimer, S. (2002). Functional fMRI of language: New approaches tounderstanding the cortical organization of semantic processing. AnnualReview of Neuroscience, 25, 151–188.

Bosman, C., García, R., & Aboitiz, F. (2004). FOXP2 and the languageworking memory system. Trends in Cognitive Sciences, 6, 251–252.

Bosman, C., López, V., & Aboitiz, F. (2005). Sharpening Occam’s razor: Isthere necessity of a hand-signing stage prior to vocal communication?Behavioral and Brain Sciences, 28, 128–129.

Brodmann, K. (1909). Vergleichende Lokalisationslehre der Gro� hirnrinde.Leipzig: Barth.

Bullier, J., Schall, J. D., & Morel, A. (1996). Functional streams in occipito-frontal connections in the monkey. Behavioral Brain Research, 76,89–97.

Calvert, G. A., Brammer, M. J., Bullmore, E. T., Campbell, R., Iversen, S.D., & David, A. S. (1999). Response ampliWcation in sensory-speciWccortices during crossmodal binding. Neuroreport, 10, 2619–2623.

Calvin, W. H. (1983). A stone’s throw and its launch window: Timing pre-cision and its implications for language and hominid brains. Journal ofTheoretical Biology, 104, 121–135.

Caplan, D. (1987). Neurolinguistics and linguistic aphasiology: An introduc-tion. Cambridge: Cambridge University Press.

Caplan, D., Alpert, N., & Waters, G. (1998). EVects of syntactic structureand propositional number on patterns of regional cerebral blood Xow.Journal of Cognitive Neuroscience, 10, 541–552.

Caplan, D., Alpert, N., Waters, G., & Olivieri, A. (2000). Activation ofBroca’s area by syntactic processing under conditions of concurrentarticulation. Human Brain Mapping, 9, 65–71.

Caplan, D., & Waters, G. S. (1999). Verbal working memory and sentencecomprehension. Behavioral and Brain Sciences, 22, 77–126.

Castiello, U. (2005). The neuroscience of grasping. Nature Reviews Neuro-science, 6, 726–736.

Cavada, C., & Goldman-Rakic, P. (1989). Posterior parietal cortex in rhe-sus monkey: II. Evidence for segregated cortico-cortical networks link-ing sensory and limbic areas with the frontal lobe. Journal ofComparative Neurology, 287, 422–445.

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 53

Chomsky, N. (1991). Linguistics and cognitive science: Problems and mys-teries. In A. Kasher (Ed.), The chomskyan turn. Cambridge, MA: Black-well.

Cooke, A., Zurif, E. B., DeVita, C., Alsop, D., Koenig, P., Detre, J., et al.(2002). Neural basis for sentence comprehension: Grammatical andshort-term memory components. Human Brain Mapping, 15, 80–94.

Culotta, E. (2005). What genetic changes made us human? Science, 309, 91.Corballis, M. C. (2003). From mouth to hand: Gesture, speech, and

the evolution of right-handedness. Behavioral and Brain Sciences, 26,199–208.

Damasio, A. R., & Tranel, D. (1993). Nouns and verbs are retrieved withdiVerently distributed neural systems. Proceedings of the NationalAcademy of Sciences of the United States of America, 90, 4957–4960.

Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D., & Damasio, A.R. (1996). A neural basis for lexical retrieval. Nature, 380, 409–505.

de Fockert, J. W., Rees, G., Frith, C. D., & Lavie, N. (2001). The role ofworking memory in visual selective attention. Science, 291, 1803–1806.

Doupe, A. J., & Kuhl, P. K. (1999). Birdsong and human speech: Commonthemes and mechanisms. Annual Review of Neuroscience, 22, 567–631.

Dronkers, N. F. (1996). A new brain region for coordinating speech articu-lation. Nature, 384, 159–161.

Dronkers, N., & Ogar, J. (2004). Brain areas involved in speech produc-tion. Brain, 127, 1461–1462.

Dronkers, N. F., Shapiro, J. K., Redfern, B., & Knight, R. T. (1992). Therole of Broca’s area in Broca’s aphasia. Journal of Clinical and Experi-mental Neuropsychology, 14, 52–53.

Dronkers, N. F., Wilkins, D. P., Van Valin, R. D., Jr., Redfern, B. B., & Jae-ger, J. J. (2004). Lesion analysis of the brain areas involved in languagecomprehension. Cognition, 92, 145–177.

Durstewitz, D., Seamans, J. K., & Sejnowski, T. J. (2000). Neurocomputa-tional models of working memory. Nature Neuroscience, 3(Suppl.),1184–1191.

Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic predictions: Oscilla-tions and synchrony in top-down processing. Nature Reviews Neurosci-ence, 2, 704–717.

Engel, A. K., & Singer, W. (2001). Temporal binding and the neural corre-lates of sensory awareness. Trends in Cognitive Sciences, 5, 16–25.

Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Vallender, E. J., Anderson,J. R., Vaez-Azizi, L. M., et al. (2005). Microcephalin, a gene regulatingbrain size, continues to evolve adaptively in humans. Science, 309,1717–1720.

Everett, D. (2004). Cultural constraints on grammar and cognition inPiraha: Another look at the design features of human language. Unpub-lished manuscript, Manchester: University of Manchester. <http://lings.ln.man.ac.uk/info/staV/DE/cultgram.pdf/>.

Fadiga, L., & Craighero, L. (2004). Electrophysiology of action representa-tion. Journal of Clinical Neurophysiology, 21, 157–169.

Falk, D. (2004). Prelinguistic evolution in early hominins: Whence mother-ese? Behavioral and Brain Sciences, 27, 491–503.

Felleman, D. J., & Van Essen, D. C. (1991). Distributed hierarchical pro-cessing in the primate cerebral cortex. Cerebral Cortex, 1, 1–47.

Ferrari, P. F., Gallese, V., Rizzolatti, G., & Fogassi, L. (2003). Mirror neu-rons responding to the observation of ingestive and communicativemouth actions in the monkey ventral premotor cortex. European Jour-nal of Neuroscience, 17, 1703–1714.

Ferreira, F., & Clifton, C. (1986). The independence of syntactic process-ing. Journal of Memory and Language, 25, 1–18.

Feyeresien, P., & Havard, I. (1999). Mental imagery and production ofhand gestures by younger and older adults. Journal of NonverbalBehavior, 23, 153–171.

Fiebach, C. J., Schelewsky, M., & Friederici, A. D. (2002). Separating syn-tactic memory costs and syntactic integration costs during parsing: Theprocessing of german Wh-questions. Journal of Memory and Language,47, 250–272.

Fiebach, C. J., Schlesewsky, M., Lohmann, G., von Cramon, D. Y., &Friederici, A. D. (2005). Revisiting the role of Broca’s area in sentenceprocessing: Syntactic integration versus syntactic working memory.Human Brain Mapping, 24, 79–91.

Fingelkurts, A., Fingelkurts, A., Krause, C., Kaplan, A., Borisov, S., &Sams, M. (2003). Structural (operational) synchrony of EEG alphaactivity during an auditory memory task. Neuroimage, 20, 529–542.

Fitch, W. T. (2000). The evolution of speech: A comparative review. Trendsin Cognitive Sciences, 4, 258–267.

Fitch, W. T., & Hauser, M. D. (2004). Computational constraints on syn-tactic processing in a nonhuman primate. Science, 303, 377–380.

Fitch, W. T., Hauser, M. D., & Chomsky, N. (2005). The evolution ofthe language faculty: ClariWcations and implications. Cognition, 97,179–210.

Frackowiak, R. S. (1994). Functional mapping of verbal memory and lan-guage. Trends in Neuroscience, 17, 109–115.

Frey, S. H., Vinton, D., Norlund, R., & Grafton, S. T. (2005). Corticaltopography of human anterior intraparietal cortex active during visu-ally guided grasping. Cognitive Brain Research, 23, 397–405.

Friederici, A. D. (2004). The neural basis of syntactic processes. In M. S.Gazzaniga (Ed.), The cognitive neurosciences III. Cambridge, MA: MITPress.

Fuster, J. M. (1995a). Memory in the cerebral cortex. Cambridge, MA:MIT Press.

Fuster, J. M. (1995b). Memory in the cortex of the primate. BiologicalResearch, 28, 59–72.

Fuster, J. M. (2003). Cortex and mind. Oxford: Oxford University Press.Fuster, J. M., & Alexander, G. E. (1971). Neuron activity related to short-

term memory. Science, 173, 652–654.Gallese, V. (2003). A neuroscientiWc grasp of concepts: From control to

representation. Philosophical Transactions of the Royal Society of Lon-don B Biological Sciences, 358, 1231–1240.

Gannon, P. J., Kheck, N. M., Braun, A. R., & Holloway, R. L. (2005). Pla-num parietal of chimpanzees and orangutans: A comparative reso-nance of human-like planum temporal asymmetry. Anatomical RecordsA. Discoveries in Molecular and Cellular Evolutionary Biology, 287,1128–1141.

Gathercole, S. E., & Baddeley, A. D. (1990). The role of phonologicalmemory in vocabulary acquisition: A study of young children learningnew names. British Journal of Psychology, 81, 439–454.

Gemba, H., Miki, N., & Sasaki, K. (1997). Cortical Weld potentials preced-ing vocalizations in monkeys. Acta Otolaryngologica Supplemental,532, 96–98.

Geschwind, N. (1965). Disconnexion syndromes in animals and man.Brain, 88, 237–294 585-644.

Gibson, E. (1998). Linguistic complexity: Locality of syntactic dependen-cies. Cognition, 68, 1–76.

Gibson, E. (2000). The dependency locality theory: A distance-based the-ory of linguistic complexity. In Y. Miyashita, A. Marantaz, & W.O’Neill (Eds.), Image, language, brain. Cambridge, MA: MIT Press.

Gil-da-Costa, R., Braun, A., Lopes, M., Hauser, M. D., Carson, R. E.,Herscovitch, P., et al. (2004). Toward an evolutionary perspective onconceptual representation: Species-speciWc calls activate visual andaVective processing systems in the macaque. Proceedings of theNational Academy of Sciences of the United States of America, 101,17516–17521.

Glassman, R. B. (2003). Topology and graph theory applied to corticalanatomy may help explain working memory capacity for three or foursimultaneous items. Brain Research Bulletin, 60, 25–42.

Goldenberg, G. (1997). Disorders of body perception. In T. E. Feinberg &M. J. Farah (Eds.), Behavioral neurology and neuropsychology. NewYork: McGraw-Hill.

Goldenberg, G. (2001). Imitation and matching of hand and Wnger pos-tures. NeuroImage, 14, S132–S136.

Goldenberg, G., & Hagmann, S. (1997). The meaning of meaningless ges-tures: A study of visuo-imitative apraxia. Neuropsychologia, 35, 333–341.

Goldin-Meadow, S., & Wagner, S. M. (2005). How our hands help us learn.Trends in Cognitive Sciences, 9, 234–241.

Goldman-Rakic, P. S. (1996). The prefrontal landscape: Implications offunctional architecture for understanding human mentation and thecentral executive. Philosophical Transactions of the Royal Society ofLondon B Biological Sciences, 351, 1445–1453.

54 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

Goldman-Rakic, P. S. (2000). Localization of function all over again. Neu-roimage, 11, 451–457.

Gottlieb, Y., Vaadia, E., & Abeles, M. (1989). Single unit activity in theauditory cortex of a monkey performing a short term memory task.Experimental Brain Research, 74, 139–148.

Grodzinsky, J. (2000). The neurology of syntax: Language use withoutBroca’s area. Behavioral and Brain Sciences, 23, 1–71.

Grodzinsky, J. (in press). A blueprint for a brain map of syntax. In K.Amunts & Y. Grodzinsky (Eds.), Broca’s area. Oxford: Oxford Univer-sity Press.

Habib, M., Demonet, J. F., & Frackowiak, R. (1996). Cognitive neuroanat-omy of language: Contribution of functional cerebral imaging. RevueNeurologique, 152, 249–260.

Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1998). Subdivisions of audi-tory cortex and ipsilateral cortical connections of the parabelt auditorycortex in macaque monkeys. Journal of Comparative Neurology, 394,475–495.

Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1999). Prefrontal connec-tions of the parabelt auditory cortex in macaque monkeys. BrainResearch, 817, 45–58.

Hagoort, P. (2003). How the brain solves the binding problem for lan-guage: A neurocomputational model of syntactic processing. Neuroim-age, 20(Suppl. 1), 18–29.

Hagoort, P. (2005). On Broca, brain, and binding: A new framework.Trends in Cognitive Sciences, 9, 416–423.

Hamilton, C. R., & Vermeire, B. A. (1988). Complementary hemisphericspecialization in monkeys. Science, 242, 1691–1694.

Hanlon, R. E., Brown, J. W., & Gerstmen, L. J. (1990). Enhancement ofnaming in nonXuent aphasia through gesture. Brain and Language, 32,298–314.

Hast, M. H., Fischer, J. M., Wetzel, A. B., & Thompson, V. E. (1974). Corti-cal motor representation of the laryngeal muscles in Macaca mulatta.Brain Research, 73, 229–240.

Hauser, M. D., Chomsky, N., & Fitch, W. T. (2002). The faculty of language:What is it, who has it, and how did it evolve? Science, 298, 1569–1579.

Henshilwood, C., d’Errico, F., Vanhaeren, M., van Niekerk, K., & Jacobs,Z. (2004). Middle Stone Age shell beads from South Africa. Science,304, 404.

Hickok, G. (2000). The left frontal convolution plays no special role insyntactic comprehension. Behavioral and Brain Sciences, 23, 35–36.

Hickok, G., Buchsbaum, B., Humphries, C., & Muftuler, T. (2003). Audi-tory-motor interaction revealed by fMRI: Speech, music, and workingmemory in area Spt. Journal of Cognitive Neuroscience, 15, 673–682.

Hickock, G., & Poeppel, D. (2000). Towards a functional neuroanatomy ofspeech perception. Trends in Cognitive Sciences, 4, 131–138.

Hillis, A. E., Work, M., Barker, P. B., Jacobs, M. A., Breese, E. L., &Maurer, K. (2004). Re-examining the brain regions crucial for orches-trating speech articulation. Brain, 127, 1479–1487.

Hopkins, W. D., & Leavens, D. A. (1998). Hand use and gestural commu-nication in chimpanzees (Pan troglodytes). Journal of Comparative Psy-chology, 112, 95–99.

Hopkins, W. D., Russell, J., Freeman, H., Buehler, N., Reynolds, E., &Schapiro, S. J. (2005). The distribution and development of handednessfor manual gestures in captive chimpanzees (Pan troglodytes). Psycho-logical Science, 16, 487–493.

Hostetter, A. B., Cantero, M., & Hopkins, W. D. (2001). DiVerential use ofvocal and gestural communication by chimpanzees (Pan troglodytes) inresponse to the attentional status of a human (Homo sapiens). Journalof Comparative Psychology, 115, 337–343.

Ide, A., Dolezal, C., Fernández, M., Labbé, E., Mandujano, R., Montes, S.,et al. (1999). Hemispheric diVerences in variability of Wssural patternsin parasylvian and cingulate regions of human brains. Journal of Com-parative Neurology, 410, 235–242.

Ide, A., Rodríguez, E., Zaidel, E., & Aboitiz, F. (1996). Bifurcation patternsin the human sylvian Wssure: Hemispheric and sex diVerences. CerebralCortex, 6, 717–725.

Izumi, A., & Kojima, S. (2004). Matching vocalizations to vocalizing facesin a chimpanzee, Pan troglodytes. Animal Cognition, 7, 179–184.

Janik, V. M. (2000). Whistle matching in wild bottlenose dolphins, Tursi-ops truncatus. Science, 289, 1355–1357.

Jarvis, E. D. (2004). Learned birdsong and the neurobiology of human lan-guage. Annals of the New York Academy of Sciences, 1016, 749–777.

Jürgens, U. (2003). From mouth to mouth and hand to hand: On languageevolution. Behavioral and Brain Sciences, 26, 229–230.

Jürgens, U., & Alipour, M. (2002). A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neu-roscience Letters, 328, 245–248.

Just, M. A., & Carpenter, P. A. (1992). A capacity theory of comprehen-sion: Individual diVerences in working memory. Psychological Review,99, 122–149.

Kaan, E., & Swaab, T. Y. (2002). The brain circuitry of syntactic compre-hension. Trends in Cognitive Sciences, 6, 350–356.

Kaas, J. H., & Hackett, T. A. (1999). ‘What’ and ‘where’ processing inauditory cortex. Nature Neuroscience, 2, 1045–1047.

King, J., & Just, M. A. (1991). Individual diVerences in syntactic compre-hension: The role of working memory. Journal of Memory and Learn-ing, 30, 580–602.

King, J. M., & Kutas, M. (1995). Who did what and when? using word-and clause-level ERPs to monitor working memory usage in reading.Journal of Cognitive Neuroscience, 7, 376–396.

Kirzinger, A., & Jürgens, U. (1982). Cortical lesion eVects and vocalizationin the squirrel monkey. Brain Research, 233, 299–315.

Kohler, E., Keysers, C., Umilta, M. A., Fogassi, L., Gallese, V., & Rizzol-atti, G. (2002). Hearing sounds, understanding actions: Action repre-sentation in mirror neurons. Science, 297, 846–848.

Krubitzer, L., & Kahn, D. M. (2003). Nature versus nurture revisited: Anold idea with a new twist. Progress in Neurobiology, 70, 33–52.

Kuhl, P. K. (1992). Psychoacoustics and speech perception: Internal stan-dards, perceptual anchors, and prototypes. In L. A. Werner & E. W.Rubel (Eds.), Developmental psychoacoustics. Washington: AmericanPsychological Association.

Kuhl, P. K. (2003). Human speech and birdsong: Communication and thesocial brain. Proceedings of the National Academy of Sciences USA,100, 9645–9646.

Kumashiro, M., Ishibashi, H., Uchiyama, Y., Itakura, S., Murata, A., &Iriki, A. (2003). Natural imitation induced by joint attention in japa-nese macaques. International Journal of Psychophysiology, 50, 81–99.

Langacker, R. W. (1987). Foundations of cognitive grammar: Theoreticalprerequisites. Stanford: Stanford University Press.

Langacker, R. W. (2000). Grammar and conceptualization. Berlin: Moutonde Gruyer.

Leavens, D. A., & Hopkins, W. D. (1998). Intentional communication bychimpanzees: A cross-sectional study of the use of referential gestures.Developmental Psychology, 34, 813–822.

Leavens, D. A., Hopkins, W. D., & Thomas, R. K. (2004). Referential com-munication by chimpanzees, Pan troglodytes. Journal of ComparativePsychology, 118, 48–57.

Levy, R., & Goldman-Rakic, P. S. (2000). Segregation of working memoryfunctions within the dorsolateral prefrontal cortex. Experimental BrainResearch, 133, 23–32.

Liebal, K., Call, J., & Tomasello, M. (2004). Use of gesture sequences inchimpanzees. American Journal of Primatology, 64, 377–396.

Liberman, A. M., & Mattingly, I. G. (1985). The motor theory of speechperception revised. Cognition, 21, 1–36.

Lieberman, P. (2002). Human language and our reptilian brain. Cambridge:Harvard Press.

MacDougall, I., Brown, F. H., & Fleagle, J. G. (2005). Stratigraphic placementand age of modern humans from Kibish, Ethiopia. Nature, 433, 733–736.

Mandler, J. M. (2004). Thought before language. Trends in Cognitive Sci-ences, 8, 508–513.

Marshall, A. J., Wrangham, R. W., & Acardi, A. C. (1999). Does learningaVect the structure of vocalizations in chimpanzees? Animal Behavior,58, 825–830.

Martin, R. C. (1987). Articulatory and phonological deWcits in short-termmemory and their relation to syntactic processing. Brain and Language,32, 159–192.

F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 55

Martin, N., & SaVran, E. M. (1997). Language and Auditory-verbal short-term memory impairments: Evidence for common underlying pro-cesses. Cognitive Neuropsychology, 14, 641–682.

Mayberry, R. I., Jacques, J., & DeDe, G. (1998). What stuttering revealsabout the development of gesture–speech relationship. New Directionsin Child Development, 79, 77–87.

Mekel-Bobrov, N., Gilbert, S. L., Evans, P. D., Vallender, E. J., Anderson,J. R., Hudson, R. R., et al. (2005). Ongoing adaptive evolutionof ASPM, a brain size determinant in Homo sapiens. Science, 309,1720–1722.

Miklósi, A. (1999). From grasping to speech: Imitation might provide amissing link. Trends in Neurosciences, 22, 151–152.

Miller, G. A., & Chomsky, N. (1963). Finitary models of language users. InD. Luce, R. Bush, & E. Galanter (Eds.), Handbook of mathematical psy-chology (Vol. 2). New York: Wiley.

Mitani, J. C., Hunley, K. L., & Murdoch, M. E. (1999). Geographic varia-tion in the calls of wild chimpanzees: A reassessment. American Journalof Primatology, 47, 133–151.

Müller, R. A. (2000). A big “housing” problem and a trace of neuroimag-ing: Broca’s area is more than a transformation center. Behavioral andBrain Sciences, 23, 42.

Müller, R. A., & Basho, S. (2004). Are nonlinguistic functions in “Broca’sarea” prerequisites for language acquisition. FMRI Wndings from anontogenetic viewpoint. Brain and Language, 89, 329–336.

Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M., & Matsuzawa, T.(2004). Imitation in neonatal chimpanzees, Pan troglodytes. Develop-mental Science, 7, 437–442.

Nelissen, K., Luppino, G., VanduVel, W., Rizzolatti, G., & Orban, G. A.(2005). Observing others: Multiple action representation in the frontallobe. Science, 310, 332–336.

Ojemann, G. A. (1978). Organization of short-term verbal memory in lan-guage areas of human cortex: Evidence from electrical stimulation.Brain and Language, 5, 331–340.

Ojemann, G. A. (1991). Cortical organization of language. Journal of Neu-roscience, 11, 2281–2287.

Ojemann, G. A. (2003). The neurobiology of language and verbal memory:Observations from awake neurosurgery. International Journal of Psy-chophysiology, 48, 141–146.

Ojemann, G. A., & Mateer, C. (1979). Human language cortex: Localiza-tion of memory, syntax, and sequential motor-phoneme identiWcationsystems. Science, 205, 1401–1403.

Ojemann, G. A., SchoenWeld-McNeill, J., & Corina, D. P. (2002). Anatomicsubdivisions in human temporal cortical neuronal activity related torecent verbal memory. Nature Neuroscience, 5, 64–71.

Okanoya, K. (2004). The Bengalese Wnch: A window on the behavioralneurobiology of birdsong syntax. Annals of the New York Academy ofSciences, 1016, 724–735.

Palva, J. M., Palva, S., & Kaila, K. (2005). Phase synchrony among neuronaloscillations in the human cortex. Journal of Neuroscience, 25, 3962–3972.

Parker, G. J. M., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A. M.,Ciccarelli, O., & Lambon Ralph, M. A. (2005). Lateralization of ventraland dorsal auditory-language pathways in the human brain. NeuroIm-age, 24, 656–666.

Pasternak, T., & Greenlee, M. W. (2005). Working memory in primate sen-sory systems. Nature Reviews Neuroscience, 6, 97–107.

Patel, A. D. (2003). Language, music, syntax and the brain. Nature Neuro-science, 7, 674–681.

Patel, A. D., Gibson, E., Ratner, J., Besson, M., & Holcomb, P. J. (1998).Processing syntactic relations in language and music: An event-relatedpotential study. Journal of Cognitive Neuroscience, 10, 717–733.

Paulesu, E., Frith, C. D., & Frackowiak, R. S. (1993). The neural correlatesof the verbal component of working memory. Nature, 362, 342–345.

Paus, T. (2001). Primate anterior cingulate cortex: Where motor control,drive and cognition interface. Nature Reviews Neuroscience, 2, 417–424.

Peigneux, P., Salmon, E., Van der Linden, M., Garraux, G., Aerts, J., DelW-ore, G., et al. (2000). The role of lateral occipitotemporal junction andarea MT/V5 in the visual analysis of upper limb postures. NeuroImage,11, 644–655.

Petrides, M. (in press). Broca’s area in the human and the non-human pri-mate brain. In K. Amunts & Y. Grodzinsky (Eds.), Broca’s area.Oxford: Oxford University Press.

Petrides, M., & Pandya, D. N. (1984). Projections to the frontal cortexfrom the posterior parietal region in the rhesus monkey. Journal ofComparative Neurology, 228, 105–116.

Petrides, M., & Pandya, D. N. (1988). Association Wber pathways to thefrontal cortex from the superior temporal region in the rhesus monkey.Journal of Comparative Neurology, 273, 52–66.

Petrides, M., & Pandya, D. N. (1999). Dorsolateral prefrontal cortex:Comparative cytoarchitectonic analysis in the human and the macaquebrain and corticocortical connection patterns. European Journal ofNeuroscience, 11, 1011–1036.

Petrides, M., & Pandya, D. N. (2001). Comparative cytoarchitectonic anal-ysis of the human and the macaque ventrolateral prefrontal cortex andcorticocortical connection patterns in the monkey. European Journal ofNeuroscience, 16, 291–310.

Petrides, M., Cadoret, G., & Mackey, S. (2005). Orofacial somatomotorresponses in the macaque monkey homologue of Broca’s area. Nature,435, 1235–1238.

Pika, S., Liebal, T., Call, J., & Tomasello, M. (in press). The gestural com-munication of apes. Gesture.

Pinker, S. (1995). The language instinct: How the mind creates language.New York: Harper Perennial.

Pinker, S., & JackendoV, R. (2005). The faculty of language: What’s specialabout it? Cognition, 95, 201–236.

Pizzamiglio, L., Aprile, T., Spitoni, G., Pitzalis, S., Bates, E., D’Amico, S., etal. (2005). Separate neural systems for processing action- or non-action-related sounds. Neuroimage, 24, 852–861.

Poole, J. H., Tyack, P. L., Stoeger-Horwath, A. S., & Watwood, S. (2005).Elephants are capable of vocal learning. Nature, 434, 455–456.

Preuss, T., & Goldman-Rakic, P. S. (1991a). Myelo and cytoarchitecture ofthe granular frontal cortex and surrounding regions in the strepsirhineprimate Galago and the anthropoid primate Macaca. Journal of Com-parative Neurology, 310, 429–474.

Preuss, T., & Goldman-Rakic, P. S. (1991b). Architectonics of the parietaland temporal association cortex in the strepsirhine primate Galagocompared to the anthropoid primate Macaca. Journal of ComparativeNeurology, 310, 475–506.

Preuss, T., & Goldman-Rakic, P. S. (1991c). Ipsilateral cortical connectionsof granular frontal cortex in the strepsirhine primate Galago, withcomparative comments on anthropoid primates. Journal of Compara-tive Neurology, 310, 507–549.

Pulvermüller, F. (1999). Words in the brain’s language. Behavioral andBrain Sciences, 22, 253–336.

Pulvermüller, F. (2005). Brain mechanisms linking language and action.Nature Reviews Neuroscience, 6, 576–582.

Pulvermüller, F., Lutzenberger, W., & Preissl, H. (1999). Nouns and verbsin the intact brain: Evidence from event-related potentials and high-frequency cortical responses. Cerebral Cortex, 9, 497–506.

Rauschecker, J. P., & Tian, B. (2000). Mechanisms and streams for pro-cessing of “what” and “where” in auditory cortex. Proceedings of theNational Academy of Sciences of the United States of America, 97,11800–11806.

Rizzolatti, G., & Arbib, M. A. (1998). Language within our grasp. Trendsin Neuroscience, 21, 188–194.

Rizzolatti, G., & Arbib, M. A. (1999). From grasping to speech: Imitation mayprovide a missing link. Reply to Miklósi. Trends in Neuroscience, 22, 152.

Rizzolatti, G. W., & Craighero, L. (2004). The mirror-neuron system.Annual Reviews in Neuroscience, 27, 169–192.

Romanski, L. M., Averbeck, B. B., & Diltz, M. (2005). Neural representa-tion of vocalizations in the primate ventrolateral prefrontal cortex.Journal of Neurophysiology, 93, 734–747.

Romanski, L. M., Bates, J. F., & Goldman-Rakic, P. S. (1999). Auditorybelt and parabelt projections to the prefrontal cortex in the rhesusmonkey. Journal of Comparative Neurology, 403, 141–157.

Romanski, L. M., & Goldman-Rakic, P. S. (2002). An auditory domain inprimate prefrontal cortex. Nature Neuroscience, 5, 15–16.

56 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

Romanski, L. M., Tian, B., Fritz, J. B., Mishkin, M., Goldman-Rakic, P. S.,& Rauschecker, J. P. (2000). ‘What, ‘where’ and ‘how’ in auditory cor-tex. Reply to Belin & Zatorre. Nature Neuroscience, 3, 966.

Romanski, L. M., Tian, B., Mishkin, M., Goldman-Rakic, P. S., & Raus-hecker, J. P. (1999). Dual streams of auditory aVerents target multipledomains in the primate prefrontal cortex. Nature Neuroscience, 2,1131–1136.

Ruchkin, D. S., Grafman, J., Cameron, K., & Berndt, R. S. (2003). Workingmemory retention systems: A state of activated long-term memory.Behavioral and Brain Sciences, 26, 709–728.

Salmon, E., Van der Linden, M., Collette, F., DelWore, G., Maquet, P., Deg-ueldre, C., et al. (1996). Regional brain activity during working mem-ory tasks. Brain, 119, 1617–1625.

Schoenemann, P. T. (1999). Syntax as an emergent characteristic of theevolution of semantic complexity. Minds and Machines, 9, 309–346.

Scott, S. K., & Johnsrude, I. S. (2003). The neuroanatomical and functionalorganization of speech perception. Trends in Neuroscience, 26, 100–107.

Seyfarth, R. M., & Cheney, D. L. (2003). Meaning and emotion in animalvocalizations. Annals of the New York Academy of Science, 1000,32–55.

Shapiro, A. D., Slater, P. J., & Janik, V. M. (2004). Call usage learning ingray seals, Halichoerus grypus. Journal of Comparative Psychology, 118,447–454.

Singer, W. (1999). Neuronal synchrony: A versatile code for the deWnitionof relations? Neuron, 24, 49–65.

Singer, W. (2001). Consciousness and the binding problem. Annals of theNew York Academy of Sciences, 929, 123–146.

Slocombe, K. E., & Zuberbuhler, K. (2005). Agonistic screams in wildchimpanzees (Pan troglodytes schweinfurthii) vary as a function ofsocial role. Journal of Comparative Psychology, 119, 67–77.

Smith, E. E., & Jonides, J. (1998). Neuroimaging analyses of human work-ing memory. Proceedings of the National Academy of Sciences of theUnited States of America, 95, 12061–12068.

Stowe, L. A. (2000). Sentence comprehension and the left inferior frontalgyrus: Storage, not comprehension. Behavioral and Brain Sciences, 23, 51.

Stromswold, K., Caplan, D., Alpert, N., & Rauch, S. (1996). Localizationof syntactic comprehension by positron emission tomography. Brainand Language, 52, 452–473.

Subiaul, F., Cantlon, J. F., Holloway, R. L., & Terrace, H. S. (2004). Cogni-tive imitation in rhesus macaques. Science, 305, 407–410.

Szelag, E., & Pöppel, E. (2000). Temporal perception: A key to understandlanguage. Behavioral and Brain Sciences, 23, 52.

Tallon-Baudry, C., Bertrand, O., & Fischer, C. (2001). Oscillatory syn-chrony between human extrastriate areas during visual short-termmemory maintenance. Journal of Neuroscience, 21, RC177.

Tallon-Baudry, C., Mandon, S., Freiwald, W. A., & Kreiter, A. K. (2004).Oscillatory synchrony in the monkey temporal lobe correlates withperformance in a visual short-term memory task. Cerebral Cortex, 14,713–720.

Tian, B., Reser, D., Durham, A., Kustov, A., & Rauschecker, J. P. (2001).Functional specialization in rhesus monkey auditory cortex. Science,292, 290–293.

Vogel, G. (1999). Chimps in the wild show stirrings of culture. Science, 284,2070–2073.

Webster, R. I., & Shevell, M. I. (2004). Neurobiology of speciWc languageimpairment. Journal of Child Neurology, 19, 471–481.

Whiten, A. (2005). The second inheritance system of chimpanzees andhumans. Nature, 437, 52–55.

Whiten, A., Horner, V., & de Waal, F. B. (2005). Conformity to culturalnorms of tool use in chimpanzees. Nature, 437, 737–740.

Wilson, S. M., Saygin, A. P., Sereno, M. I., & Iacoboni, M. (2004). Listeningto speech activates motor areas involved in speech production. NatureNeuroscience, 7, 701–702.

Wise, R. J., Scott, S. K., Blank, S. C., Mummery, C. J., Murphy, K., & War-burton, E. A. (2001). Separate neural subsystems within ‘Wernicke’sarea’. Brain, 124, 83–95.

Yuste, R., MacLean, J. N., Smith, J., & Lansner, A. (2005). The cortex as acentral pattern generator. Nature Reviews Neuroscience, 6, 477–483.

Zatorre, R. J., & Belin, P. (2001). Spectral and temporal processing inhuman auditory cortex. Cerebral Cortex, 11, 946–953.