Cognitive Neuropsychology - Research Explorer

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This article was downloaded by:[The University of Manchester] On: 26 July 2007 Access Details: [subscription number 773564139] Publisher: Psychology Press Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Cognitive Neuropsychology Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713659042 Semantic memory is an amodal, dynamic system: Evidence from the interaction of naming and object use in semantic dementia Michela Coccia a ; Marco Bartolini a ; Simona Luzzi a ; Leandro Provinciali a ; Matthew A. Lambon Ralph b a Ospedale Umberto I, Ancona, Italy b University of Manchester, Manchester, UK Online Publication Date: 01 July 2004 To cite this Article: Coccia, Michela, Bartolini, Marco, Luzzi, Simona, Provinciali, Leandro and Ralph, Matthew A. Lambon (2004) 'Semantic memory is an amodal, dynamic system: Evidence from the interaction of naming and object use in semantic dementia', Cognitive Neuropsychology, 21:5, 513 - 527 To link to this article: DOI: 10.1080/02643290342000113 URL: http://dx.doi.org/10.1080/02643290342000113 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. © Taylor and Francis 2007

Transcript of Cognitive Neuropsychology - Research Explorer

This article was downloaded by:[The University of Manchester]On: 26 July 2007Access Details: [subscription number 773564139]Publisher: Psychology PressInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Cognitive NeuropsychologyPublication details, including instructions for authors and subscription information:http://www.informaworld.com/smpp/title~content=t713659042

Semantic memory is an amodal, dynamic system:Evidence from the interaction of naming and object usein semantic dementiaMichela Coccia a; Marco Bartolini a; Simona Luzzi a; Leandro Provinciali a;Matthew A. Lambon Ralph ba Ospedale Umberto I, Ancona, Italyb University of Manchester, Manchester, UK

Online Publication Date: 01 July 2004To cite this Article: Coccia, Michela, Bartolini, Marco, Luzzi, Simona, Provinciali,Leandro and Ralph, Matthew A. Lambon (2004) 'Semantic memory is an amodal,dynamic system: Evidence from the interaction of naming and object use in semanticdementia', Cognitive Neuropsychology, 21:5, 513 - 527

To link to this article: DOI: 10.1080/02643290342000113URL: http://dx.doi.org/10.1080/02643290342000113

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf

This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction,re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expresslyforbidden.

The publisher does not give any warranty express or implied or make any representation that the contents will becomplete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should beindependently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings,demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with orarising out of the use of this material.

© Taylor and Francis 2007

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SEMANTIC MEMORY IS AN AMODAL, DYNAMIC

SYSTEM: EVIDENCE FROM THE INTERACTION OF

NAMING AND OBJECT USE IN SEMANTIC DEMENTIA

Michela Coccia, Marco Bartolini, Simona Luzzi, and Leandro ProvincialiOspedale Umberto I, Ancona, Italy

Matthew A. Lambon RalphUniversity of Manchester, Manchester, UK

Classic neurological accounts and some contemporary theories of semantic memory assume thatconcepts are acquired through a learning process that draws together information experienced in each ofour verbal and nonverbal modalities. These accounts embody three critical assumptions: semanticrepresentations are amodal; the mapping between surface form and meaning varies for differentmodalities; and the representations are dynamic. The influence of these three factors was revealed indata collected over a 4-year longitudinal period in two patients with semantic dementia. Semanticassessment revealed a parallel decline in verbal and nonverbal aspects of conceptual knowledge,reflecting a gradual degradation of a single amodal semantic system. As expected, when the patients’semantic impairment was mild, they presented with profound anomia but relatively preserved objectuse. Over time, performance on all semantic tasks including object use declined. High item-by-itemconsistency across these tasks was observed in all testing sessions. The impact of dynamic semanticrepresentations was revealed by a striking clinical finding. Although unable to name many of the objectsin isolation, their performance was significantly facilitated if they were asked to name while theydemonstrated the use of each object. These results are discussed in the context of contemporary modelsof semantic memory.

INTRODUCTION

Warrington (1975) was the first in the cognitiveneuropsychology literature to describe patients whohad a selective impairment of semantic memory orconceptual knowledge. More recent studies haveconfirmed that these patients—those withsemantic dementia—do have a selective andprogressive impairment of conceptual knowledgethat spares many other aspects of cognition includ-ing nonverbal problem-solving, visuospatial skills,

orientation for time and place, memory for currentevents, single-word phonology, and expressive andreceptive syntax (Hodges, Garrard, & Patterson,1998; Hodges, Patterson, Oxbury, & Funnell,1992; Snowden, Goulding, & Neary, 1989).Although semantic deficits are found in otheraetiologies (CVA: Chertkow, Bub, Deaudon, &Whitehead, 1997; AD: Hodges & Patterson, 1995;HSVE: Wilson, 1997), assessment is alwaysclouded by other concomitant cognitive and lan-guage impairments. Semantic dementia represents,

COGNITIVE NEUROPSYCHOLOGY, 2004, 21 (5), 513–527

� 2004 Psychology Press Ltdhttp://www.tandf.co.uk/journals/pp/02643294.html DOI:10.1080/02643290342000113

513

Correspondence should be addressed to Prof M. A. Lambon Ralph, Dept of Psychology, University of Manchester, Oxford Road,Manchester M13 9PL, UK (Email: [email protected]), or to Dr Simona Luzzi, Dipartimento di Scienze Neurologiche,Ospedale Umberto I, Torrette, 60020 Ancona, Italy (Email: [email protected]).

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therefore, one of the best patient models withwhich to explore the nature of semantic breakdown,the organisation of conceptual knowledge and,through its interaction with other cognitivesystems, the influence of semantic memory onverbal and nonverbal tasks. The present study isconcerned primarily with the internal structure ofsemantic memory and the interactions that supportverbal (e.g., naming) and nonverbal activities (e.g.,object use).

The Wernicke-Meynert theory of semanticmemory assumed that conceptual representationsare the conjoint activation of information withinperceptual and motor association cortices (Eggert,1977). In a similar vein, Allport (1985) proposedthat concepts are acquired through a Hebbian-likelearning process that draws together informationexperienced in each of our verbal and nonverbalmodalities. The concept of telephone, for example,comprises information acquired through each ofthe modalities in which we experience this object(auditory, haptic, visual, and verbal). The theoryproposed by Damasio and colleagues (Damasio,Grabowski, Tranel, Hichwa, & Damasio, 1996;Tranel, Damasio, & Damasio, 1997) builds uponthis traditional neurological approach by assumingthat constituent semantic features are stored withinprimary association areas but they are indexed orlinked via nodes stored within temporal loberegions. A specific role for temporal areas isintriguing given that patients with semanticdementia do not have widespread damage to allprimary association areas but instead have relativelycircumscribed atrophy of the inferolateral, polartemporal region bilaterally, including the inferiortemporal lobe gyrus (Galton et al., 2001;Mummery, Patterson, Price, Ashburner,Frackowiak, & Hodges, 2000).

Rogers et al. (in press) used an implementedparallel distributed processing model that drawstogether known neuroanatomy and neuropsychol-ogy to provide a comprehensive description ofsemantic memory and its breakdown, as observed inpatients with semantic dementia. Like previousproposals, this model assumed that semanticrepresentations reflect the totality of our verbaland nonverbal experience with each concept. The

model was trained to take one form of input (e.g., avisual representation) and, via a set of mediatinghidden units, to reproduce correct informationabout that concept (e.g., its name, propositionalfeatures, etc.). Through a gradual learning processthat required all information about each concept tobe activated from any input, abstract semanticrepresentations were formed across these hiddenunits. When the connections to the hidden unitswere damaged, the model was able to reproduce awide variety of semantic dementia data. Although afull summary of this computational model isbeyond the scope of the present paper, the simula-tion captured three critical assumptions that arecentral to the present study: semantic representa-tions are amodal; the mapping between surfaceform and meaning varies for different modalities;and the representations are dynamic. All threeassumptions are not unique to this computationalmodel. They are also central characteristics of otherneuropsychological models of semantic memory,most notably, the Organised Unitary ContentHypothesis (OUCH; Caramazza, Hillis, Rapp,& Romani, 1990; Hillis, Rapp, Romani, &Caramazza, 1990; Rapp, Hillis, & Caramazza,1993). Each of these assumptions is discussedbelow.

A central tenet of OUCH is that semantic repre-sentations are stored within a single system that isnot specific to any modality (Caramazza et al.,1990; Hillis et al., 1990; Rapp et al., 1993). In thecomputational framework, all translations withinand between verbal and nonverbal representationsare mediated by the same set of hidden units. In thisway, the model implements the same assumption asOUCH; that the intermediate semantic represen-tations are a single, amodal system. The knownneuroanatomy for the inferolateral temporalregions supports this architectural choice in thesimulation of semantic dementia: These neuralregions have extensive afferent and efferent con-nections to the association and classical languagecortices (Gloor, 1997). This, in turn, leads to theprediction that damage to the semantic system willhave an impact upon all semantic tasks in anymodality. Previous studies of patients withsemantic impairment, consequent on CVA, have

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shown that performance was equivalent acrossmany types of task (e.g., patient KE; Hillis et al.,1990). Likewise, case-series studies of patients withsemantic dementia have confirmed this prediction(Bozeat, Lambon Ralph, Patterson, Garrard, &Hodges, 2000). Patients demonstrate impairmentson verbal and nonverbal receptive and expressivetasks that are commensurate with the severity ofsemantic impairment in each case.

In contrast to the position adopted by OUCHand the computational model, other researchershave argued in favour of modality-specific semanticsystems. Two lines of evidence have been used infavour of the multiple semantic systems position.First, there are patients who demonstrate differentlevels of performance across tasks/modalities(McCarthy & Warrington, 1988; Shallice, 1988).These differences are readily explained by assumingthat such patients have impairments within one ofthe multiple semantic systems. Second, modality-specific semantic systems have also been posited toexplain category-specific semantic impairments.While a full discussion of this literature is beyondthe scope of this paper (for recent reviews andcounter-arguments, see Caramazza & Shelton,1998; Lambon Ralph, Howard, Nightingale, &Ellis, 1998), it is important to note that bothcomputational models of category specificity andrelated functional neuroimaging studies haveargued in favour of modality-specific representa-tions (Farah & McClelland, 1991; Martin, Wiggs,Ungerleider, & Haxby, 1996).

There are at least two ways in which variationacross tasks can be explained within a unitarysystem account. First, different levels of perfor-mance might reflect damage to the specific linkbetween an amodal semantic system and themodality in question. Second, the adoption of asingle, amodal system does not mean that semanticimpairments will lead to equally affected perfor-mance across different tasks. Accuracy on anyparticular activity (e.g., naming and object use) willbe dependent not only on the degree of semanticimpairment but also on the nature of the mappingbetween semantic memory and the surface repre-sentations engaged in a particular task. This notionwas encapsulated within OUCH in terms of the

assumptions of privileged access and privileged rela-tionships (Rapp et al., 1993). In addition, there arenow a number of implemented PDP modelsdemonstrating that the accuracy of semantic activa-tion is dependent upon the nature of the mapping(Lambon Ralph & Howard, 2000; Plaut, 1999;Rogers et al., in press). Both OUCH and thecomputational models can be summarised in thesame way. If there is no clear relationship betweenrepresentations—an arbitrary mapping—thenperformance is extremely sensitive to semanticdamage. In contrast, performance is much moreresilient if the mapping is systematic—where thereare corresponding or correlated elements betweenrepresentations. These differences can explain whysome semantically impaired patients are worse onverbal than nonverbal comprehension withoutpositing a division within the semantic system itself(Bozeat et al., 2000; Caramazza et al., 1990; Hillis,Rapp, & Caramazza, 1995; Lambon Ralph &Howard, 2000). Likewise, part of the reason whyanomia is so pronounced, even in patients with mildcomprehension impairments, is the arbitrary rela-tionship between semantic and phonological repre-sentations (Lambon Ralph, McClelland,Patterson, Galton, & Hodges, 2001).

The impact of semantic impairment on objectuse is theoretically and clinically important. Ifsemantic impairment leads to poor object use thenthis should impact on activities of everyday living.Our working hypothesis is that single object use issupported by two routes from vision to motorsystems (Hodges, Spatt, & Patterson, 1999; Milner& Goodale, 1995). One route represents a directcomputation of praxis from visual input, whichencompasses aspects of use that are directlyafforded by an object’s structure. The second routerequires activation of object meaning. The distinc-tion between praxis (i.e., how to manipulateobjects) and semantic memory is supported byreported dissociations between these types ofknowledge (Buxbaum & Saffran, 2002). Bystudying object use in semantic dementia, it ispossible to reveal the relative importance of thecontributions made by semantics and affordances.Two initial studies and clinical observationssuggested that patients with semantic dementia

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could use objects and perform a variety of activitiesof everyday living (Buxbaum, Schwartz, & Carew,1997; Lauro-Grotto, Piccini, & Shallice, 1997;Snowden, Neary, & Mann, 1996). Using a carersurvey, a recent study found that, althoughsemantic dementia patients do complete a smallnumber of the most common tasks (e.g., groomingand eating), the repertoire of domestic activities issubstantially reduced (Bozeat, Lambon Ralph,Patterson, & Hodges, 2002a). More recent experi-mental investigations that have assessed use andknowledge on the same set of objects have found avery strong relationship between the degree ofsemantic impairment and accuracy of object use(Bozeat, Lambon Ralph, Patterson, & Hodges,2002b; Hodges, Bozeat, Lambon Ralph,Patterson, & Spatt, 2000). In addition, Bozeat et al.(2002b) found that the patients’ naming of thesame objects was much worse (often at floor). Thisfollows from the functions that relate semanticimpairment to object use and naming: While thereis a strong linear relationship between semanticsand use (Bozeat et al., 2002b; Hodges et al., 2000),the relationship for naming is nonlinear, such thatmild semantic impairment produces amplifiedlevels of anomia (Lambon Ralph et al., 2001). Aninterpretation of this difference is that it reflectstwo factors noted above. First, the relationshipbetween the structural aspects of objects andmeaning is quasi-systematic whilst semantics andphonology are arbitrarily related (Lambon Ralph &Howard, 2000; Rapp et al., 1993). Second, inaddition to semantic representations driving objectuse, there are direct vision-to-motor translations(affordances) that contribute to object use (Bozeatet al., 2002b; Milner & Goodale, 1995). Incontrast, there is only semantic input for naming.

The third assumption in OUCH and the Rogerset al. model of conceptual knowledge is that theserepresentations are dynamic and not entirely fixedin nature. As noted by Rapp et al. (1993), even in aunitary system the semantic information activatedby various inputs will vary and will be coloured bythe nature of the input modality and context. Thisobservation was supported by results from acombined neuropsychological and computationalinvestigation. Lambon Ralph and Howard (2000)

found that IW, a patient with semantic dementia,was (a) consistently worse when semantics wererequired to interact with verbal representations(e.g., word definition and the word version of thePyramids and Palm Trees test—PPT: Howard &Patterson, 1992) than when activated by pictures(e.g., picture definition and the picture version ofthe PPT); but, (b) although certain meaningsseemed to be consistently unavailable to her fromverbal-only input, her comprehension wasimproved with simultaneous verbal and picturepresentation (e.g., the target word plus a semanticrelated picture). The model demonstrated exactlythe same behaviour. Activation of semantic repre-sentations was significantly worse for word thanpicture input because the model incorporated botharbitrary (for word input) and quasi-systematic (forpicture input) mappings. The consequence of anarbitrary mapping is that a relatively inaccurate/impoverished activation of the meaning is achievedfollowing damage to the semantic system. Thesame verbal input is much more effective, however,if the semantic system is first activated by a pictorialinput (even one that is only approximately semanti-cally related). The patient and model suggest thatalthough conceptual knowledge is representedwithin a single amodal system, the activatedmeaning is influenced by the form of input and thecontext. In short, conceptual representations aredynamic.

The present study reports longitudinal datafrom two patients with semantic dementia. Bothpatients were tested longitudinally on a neuro-psychological battery that included variousmeasures of semantic memory and the ability toperform certain tasks, using the same set of objects(in a similar fashion to previous studies: e.g.,Hodges et al., 2000). Specifically, the batteryincluded measures of naming, comprehension, andobject use. Like previous reports (Bozeat et al.,2002b), when these patients had a mild impairmentof comprehension, their object use was good buttheir naming of the same items was poor. Overtime, further semantic deterioration was coupledwith increasing problems with object use. Thestriking and novel finding from these two patientsis that, when their semantic impairment was

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relatively mild, although unable to name manyobjects in isolation, they were able to name asignificantly greater number of the objects whilstthey demonstrated the correct use.

CASE STUDIES

Elvezio was a 62-year-old right-handed man with13 years of education who worked as an employee inan insurance company. He presented in 1998 with a1-year history of progressive word-finding difficul-ties. During this first clinical interview, hisspontaneous speech was found to be fluent withsporadic semantic paraphasias and word-findingdifficulties. No phonological nor syntactical errorswere observed. At this time, subtle and vaguebehavioural changes, including anxiety, were noted.Elvezio’s semantic impairment had becomemore apparent following a surgical operation(haemorrhoidectomia) in 1997. The post-operativephase was complicated by copious bleeding.Elvezio’s wife tried to persuade him to call thedoctor but Elvezio responded, “Blood? What is it?I never heard this word. What is it used for? Try tospeak properly, please.”

Family and personal histories were unremark-able. General, neurological, and psychiatric exami-nations were in the normal range. Blood screeningfor dementia (cell blood count, thyroid function,immunitary profile, B12 vitamin and folic acid,syphilis serology) excluded symptomatic cognitiveimpairment. An MRI showed mild diffuse atrophywith prevalent involvement of the temporal lobes,more marked on the left than the right. AHMPAO SPECT revealed left temporal lobehypoperfusion (Figure 1).

Elvezio was clinically reviewed again in 1999.Word-finding difficulties and semantic para-phasias had become more common in his sponta-neous speech. There were no phonological orsyntactical errors. Relatives reported that he wasstill able to perform activities of daily living. He wasstill working during this period although colleagueshad started to notice that Elvezio had occasionalproblems in understanding what they said to him.

Psychiatric and neurological examinations werenormal.

By 2000, Elvezio’s spontaneous speech wasseverely compromised by word-finding difficultiesand semantic paraphasias. He had clear difficultiesunderstanding complex phrases and commands. Athome he was still autonomous and able to usevarious objects correctly. His poor verbal compre-hension compromised his ability to complete tasksto verbal command but he was able to comply if theobjects and tools were given to him. For example,when his wife asked him to hang a picture on thewall he didn’t do anything but when given ahammer, the nail and picture he hung it withoutdifficulty. His receptive and expressive languageimpairments severely compromised his ability atwork. Neurological and psychiatric examinationswere still normal.

When seen again in 2001, Elvezio’s conditionwas significantly worse. Although grammaticallyand prosodically normal, his spontaneous speechwas almost contentless, with severe word-findingdifficulties and empty circumlocutions. At work hewas reduced to performing calculations and othersmall activities. Behavioural changes were alsonoted. He had developed a mild Kluver-Bucysyndrome with compulsive food intake and a mild

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Figure 1. SPECT scans for Elvezio.

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verbal dysinhibition. Neurological examinationwas still normal.

The second case, Dirce, was a 72-year-old right-handed woman with 5 years of education. Shepresented in 1997 with a history of anomia.Although an accomplished gardener, her familyhad noticed that she wasn’t able to remember thename of plants and flowers, and sometimesproduced semantic paraphasias for these items(e.g., rose � “carnation”). Clinical assessmentrevealed that her spontaneous speech was fluent,with sporadic word-finding difficulties andsemantic paraphasias. Neither phonological norsyntactical errors were noted. Neurological andpsychiatric assessments were normal, and personaland family histories were unremarkable. Bloodscreening for dementia excluded treatable causes ofcognitive impairment. An MRI showed modestdiffuse atrophy with prominent involvement ofthe temporal lobes bilaterally. A HMPAOSPECT showed left temporal lobe hypoperfusion(Figure 2).

By 1998, Dirce’s spontaneous speech hadbecome more impoverished, with more frequentword-finding difficulties and semantic paraphasias.Phonological and syntactical errors were absent.Her relatives reported that she was still completely

self-sufficient in daily activities and houseworkchores and often went for walks unaccompanied.She refused to do shopping. Psychiatric and neuro-logical examinations were normal.

When seen again in 1999, her language functionhad declined significantly. She was unable tounderstand complex phrases or commands whileher speech was replete with word-finding pausesand semantic paraphasias. At home she was stillself-sufficient and able to use various objectscorrectly even though she was unable to name themor describe their use. Psychiatric and neurologicalexaminations were still normal.

By 2000 her overall condition had declinedconsiderably. Verbal interaction was almost impos-sible. She was disoriented and her spontaneousspeech was contentless—characterised by grossword-finding difficulties, semantic paraphasias,and empty circumlocutions. All activities at homehad to be supervised by carers. Her behaviour hadalso changed: She had developed a Kluver-Bucysyndrome with hyperorality plus exhibited aggres-siveness, irritability, and wandering behaviour.

INVESTIGATION

General neuropsychology

The following battery of neuropsychological testswas administered longitudinally to both patients.Dirce’s behavioural problems together with herattentional deficit, exhibited on her last examina-tion in 2000, made it hard to administer thecomplete test battery. A general measure of cog-nitive status was obtained by the Mini-MentalState Examination (MMSE; Folstein, Folstein,& McHugh, 1975) and the Raven’s ColouredProgressive Matrices (Raven, 1962). Executivefunctions were examined using the Visual SearchTest (Spinnler & Tognoni, 1987), Luria’s MotorSequences (Piccirilli, Piccinin, D’Alessandro,Finali, & Agostini, 1989), and the Trail MakingTest (Retain, 1958). Working memory wasassessed by the Corsi block tapping task andbisyllabic word repetition (Spinnler & Tognoni,1987). Long-term memory was examined using the

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Figure 2. SPECT scans for Dirce.

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Rey auditory verbal learning test (Caltagirone,Gainotti, Masullo, & Miceli, 1979), Rey-Osterrieth Figure “B” long-term retrieval (Lezak,1976), the Prose Test, and Supra Span Sequences(Spinnler & Tognoni, 1987). The patients’ scoreswere compared to age- and education-matchednormative data for these assessments.

General language assessment included theToken Test (De Renzi & Vignolo, 1962), verbalfluency for categories (Spinnler & Tognoni, 1987),the Controlled Word Association Task (F, A, Sletter fluencies; Lezak, 1976), and the Sartorireading test (Sartori, 1984). Visuoperceptual skillswere examined by the Overlapping Figures Test(Gainotti, D’Erme, Monteleone, & Silveri, 1986).Visuospatial abilities were assessed by Kohs Blocks(Wechsler, 1955) and constructional apraxia wasevaluated by copying the Rey-Osterrieth Figure(Lezak, 1976). Ideomotor and bucco-linguo-facial

praxias were evaluated according to the De Renziand Faglioni test (De Renzi & Faglioni, 1996).

As shown in Table 1, there were no signs ofgeneral cognitive impairment in either patients’longitudinal neuropsychology, with the exceptionof Dirce’s last examination in 2000. Executivefunctions, visuoperceptual and visuospatial abili-ties, constructional, ideomotor, and bucco-linguo-facial praxias, working memory, and long-termspatial memory were in the normal range. Verballong-term memory was in the normal range in thefirst examination for both patients but the scoresdeclined over time.

General language examination showed goodperformance on the Token Test. Although therewas a mild decline in scores over time, FAS letterfluency fell into the normal range for all sessionsexcept for Dirce’s last score. Category fluency wasabnormal throughout. A pattern of surface dyslexia

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Table 1. General neuropsychology

Elvezio Dirce

Test (maximum score) 1998 1999 2000 2001 1997 1998 1999 2000

MMSE (30)Raven’s Coloured Progressive Matrices (36)Visual Search (60)Trail Making Test ATrail Making Test BKohs Blocks (48)Luria’s Motor Sequences (15)

25326042564815

15a

326045604815

10a

305750844415

8a

295453904415

27274375

1504015

25274582

1784015

15a

2540

138NT4015

4a

1820a

NTNT30NT

Bisyllabic word spanCorsi’s blocksRey AVLT total effect (75)Rey AVLT long term (15)Corsi’s SupraspanRey Figure Delayed Recall (31)

55

331419.3831

55

23a

919.1031

55

18a

819.0030

55

15a

719.0030

44

321017.8121

44

23a

819.1020

44

15a

5a

17.1419

3a

4NTNTNTNT

Verbal fluency for categoriesFASToken Test (36)

25a

3535

10a

2535

10a

2134

8a

19a

32

333031.5

142530

91823

09a

NT

Rey Figure Test copy (31) 31 31 31 31 31 29 29 25

Ideomotor praxia (20)Bucco-linguo-facial praxia (20)

2020

2020

2020

2020

2020

2020

2020

18a

17a

Overlapping Figure Test (9) 9 9 8 8 9 8 8 8

NT: not tested.a pathological performance.

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was demonstrated by both patients on all fouroccasions.

Assessment of semantic memoryThe general semantic battery used the same 42items for all assessments: 21 selected from threeanimate categories (land animals, sea creatures, andbirds) and 21 from three artefact categories(vehicles, musical instruments, and householditems). For each category, both patients were askedto complete the following tasks:

1. Naming colour photographs of the 42 items.2. Category fluency—1 min for each of the six

categories.3. Picture sorting at the superordinate and

category levels.4. Drawing each of the 42 items from memory

(a correct score was given if two markersjudged the picture to have uniquely identi-fied the target object).

5. Verbal definition for each of the 42 itemsfrom the spoken name (a correct score wasgiven for definitions that contained uniquelyidentifying information).

In addition, associative semantic knowledge wasassessed using an Italian version of the Pyramidsand Palm Trees Test (Howard & Patterson, 1992)in which the subject is asked to pick one of fouritems that is most closely associated with the targetconcept. The patients’ performance was comparedto that of 20 age- and educated-matched controlparticipants. Normal controls performed at ceilingacross all tasks. For the category fluency subtest,control data was taken from Hodges et al. (1992).The controls in that study produced a total meanof 47.5 items (SD = 8.9) for the three animatecategories and 49.9 (SD = 9.5) for the man-madecategories.

The patients’ scores on these semantic tests areshown in Table 2. Both Elvezio and Dirce showed

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Table 2. Results on the assessment of semantic knowledgea

Elvezio Dirce

Test (maximum score) 1998 1999 2000 2001 1997 1998 1999 2000

SortingBy domain (42)By category (42)

3827

2322

1920

1619

3829

3827

3218

193

Category fluencyLand animalBirdsWater animalVehiclesMusical instrumentsHousehold

22534514

9311301

6211101

3110100

30533676

12311223

6111111

0000000

Naming (21)LivingArtefacts

1468

844

523

101

1358

1147

624

000

Drawing from memory (21)LivingArtefacts

209

11

1257

835

312

505

303

303

000

Verbal definition (21)LivingArtefacts

133

10

817

202

000

826

716

413

000

Italian PPT (30)b

12 8 5 5 12 8 5 0

a Controls perform at ceiling on all tasks. See text for category fluency control data.b Pyramids and Palm Trees Test.

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impaired performance on all subtests that declinedin parallel over time. The combination of semanticdeficits and preserved performance on other aspectsof cognitive tasks (see Table 1) is the standardpattern for semantic dementia (Hodges et al., 1992;Snowden et al., 1989). These results also replicatethe finding that both verbal and nonverbal aspectsof conceptual knowledge are compromised insemantic dementia, and support the notion thatthese patients suffer from a progressive impairmentto an amodal semantic system (Bozeat et al., 2000).

Assessment of object use and knowledgeIn order to compare directly across differentmeasures of object use and knowledge, a batteryassessing the same 20 common objects wasconstructed.1 The battery contained the followingsubtests.

1. Naming of the 20 objects in four differentconditions: (a) visual naming—naming the visualpresented object; (b) tactile naming—naming eachobject from touch and without vision; (c) namingduring use—the patients were asked to name theitem whilst demonstrating the use of an object;(d) naming during pantomime—the patients wereasked to name the item whilst pantomiming the useof an object.

2. Single object use: the patient was asked tograsp the object and to demonstrate how the objectis usually manipulated.

3. Pantomiming the use of each object in twodifferent conditions: (a) visual pantomime—theobject was visually presented and the patient wasasked to demonstrate its use without holding theobject (i.e., mime); (b) pantomime-to-name—thepatient was told the name of an object and asked tomime its use.

4. Description of object use in two differentconditions: The patient was asked to describe howone uses each object in as much detail as possible.They described the use of either the visually

presented object (visual description) or its spokenname (description-to-name).

Each subtest was administered in a separate session,twice a day for four consecutive days. The followingorder was used in test administration: visual nam-ing, tactile naming, visual pantomime and namingduring pantomime, object use and naming duringuse, pantomime-to-name and finally the verbaldescription tasks. Naming, object use, and panto-mimes were scored as correct or incorrect. Arelatively strict criterion was adopted for scoringobject use and pantomime. The full use of eachobject had to be demonstrated for a correct score tobe given. If the demonstration contained somecorrect elements as well as some intrusive oromitted components, then the use or pantomimewas scored as incorrect. The description of objectuse was scored using a 4-point scale. Three pointswere awarded for a correct description containingspecific details (e.g., knife: “it is used to cut foodwhen you are cooking or having a meal”). Twopoints were given for a correct descriptioncontaining little or no detail (e.g., knife: “it is used tocut something”). One point was awarded whenthere was little or no information about the use perse but other correct semantic facts were provided(e.g., knife: “it’s on the table when you eat, you useit”). No points were given if the patient failed togive any information or the description was incor-rect. The patients’ performance on each subtest wascompared against that of 20 age- and education-matched control participants. These controlsubjects performed at ceiling for all tasks.

Elvezio’s and Dirce’s longitudinal object use andknowledge data is shown in Table 3. The patterndemonstrated by both patients was very similar.Over time, both patients’ scores for all measuresdeclined in parallel. This is consistent with thenotion that an amodal semantic impairment shouldgive rise to deficits in naming, object use, and verbaldefinitions (Bozeat et al., 2002b; Hillis et al., 1990;Lambon Ralph & Howard, 2000). Visual and

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SEMANTIC MEMORY: AMODAL AND DYNAMIC

1 Items included in the object use and knowledge tests: glass, pipe, whistle, toothbrush, stamp, harmonica, mask, knife, comb,scissors, brush, spoon, fork, sponge, plate, pen, screwdriver, lighter, syringe, match.

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tactile naming were moderately to severelyimpaired for both patients on all testing sessions. Instark contrast, naming during use and pantomimewas initially close to the normal range (i.e., a perfectscore) for Dirce and only mildly impaired forElvezio. Over time all naming scores declined butthe difference between visual/tactile naming andnaming during use/pantomime remained through-out. All possible pairwise comparisons betweenvisual/tactile naming versus naming during use/pantomime for the first 3 years of assessment(before performance fell to zero) confirmed that thedifferences were significant (McNemar, Exact pbetween .02 and < .001).

Initially both patients performed quite well,albeit not perfectly, when asked to demonstrate useirrespective of the condition (object use, panto-mime, or pantomime-to-name). Over time bothpatients’ scores declined in parallel for each of thethree conditions. The verbal descriptions of objectuse (to the visually presented object or its spokenname) were impoverished even at the first testinground. Like all other scores these declined overtime.

If the patients’ impaired performance on nam-ing, demonstrating use, and verbal description wasunderpinned by a progressive impairment to a

single, amodal semantic system then one mightexpect significant item-by-item associations acrossthe different modalities tested for each task(Lambon Ralph, Graham, Patterson, & Hodges,1999; Lambon Ralph & Howard, 2000). Thisfollows if we assume that different modalities accessbasically the same semantic representations. If onefinds that a certain set of concepts are degradedthrough testing in one modality, then these repre-sentations should also be affected, at least to someextent, in all other modalities. This proved to betrue for Elvezio and Dirce. For naming, there weresignificant item associations between visual andtactile naming, and between naming during use andduring pantomime (over the first three testingsessions: C between .417 and .707, p between .04and < .001).2 The only exception was the relation-ship between naming during use and during panto-mime for Elvezio in 2000 (C = .378, p = .07).Likewise for the three versions of demonstratingobject use, there were substantial item-by-itemassociations (C between .417 and .707, p between.04 and < .001). The same pattern held whenthe scores for describing the use of a visually-presented object were compared with description-to-name (� between .30 and .72, p between .03 and< .001).

522 COGNITIVE NEUROPSYCHOLOGY, 2004, 21 (5)

COCCIA ET AL.

Table 3. Performance on the object use and knowledge batterya

Elvezio Dirce

Test 1998 1999 2000 2001 1997 1998 1999 2000

Visual namingTactile namingUse namingPantomime naming

109

1619

53

1214

208

10

0045

88

1718

76

1516

44

1111

0045

UseVisual pantomimePantomime-to-name

161917

121411

81011

656

171817

161716

131111

550

Visual descriptionb

Description-to-nameb

5 (16)6 (17)

2 (14)2 (13)

2 (11)2 (13)

0 (12)0 (12)

4 (18)4 (17)

3 (17)2 (17)

0 (12)0 (11)

NTNT

a Controls perform at ceiling on all tasks.b x (y): x = number of items with score = 3; y = number of items with score = 0, 1, and 2.NT: not tested.

2 For a 2 � 2 table, the maximum value of C is .707.

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DISCUSSION

In this study, the relationship between semanticknowledge, object use, and naming was investi-gated over a 4-year longitudinal period in twopatients with semantic dementia. Until very late inthe course of their disease both patients demon-strated the typical pattern of preserved cognitive,executive, and visuospatial skills in the face ofprogressive semantic deterioration. Longitudinalsemantic assessment revealed a parallel decline inverbal and nonverbal aspects of conceptual knowl-edge. This was true for both receptive and expres-sive tasks that require semantic memory: Thepatients demonstrated increasing problems withcomprehension of pictures and words, increasinganomia, and impoverished drawings and verbaldefinitions. This pattern was replicated on aseparate neuropsychological battery designed toassess use and knowledge for the same set of 20objects. Over the 4-year period both patientsdemonstrated a yoked decline in visual and tactilenaming, demonstrating use, and describing thefunction of objects from visual presentation or theirspoken name. Over and above this parallel declinein performance, the patients exhibited consistentdifferences between modalities. Specifically, visualand tactile naming was worse than their ability todemonstrate the use of the same objects. Also, thepatients were unlikely to produce detailed, specificdescriptions of the objects’ function. Perhaps moststrikingly, we found that the patients’ naming wassignificantly facilitated by demonstration of objectuse (either with the object in hand or throughmime)—in fact their scores for naming during use/miming were the same as for object use itself.

These longitudinal results replicate and extendprevious cross-sectional and single-case studies ofpatients with semantic dementia. Previousinvestigations (Bozeat et al., 2000; Bozeat et al.,2002b; Hodges et al., 2000; Lambon Ralph et al.,1999; Lambon Ralph & Howard, 2000) havedemonstrated by-item and by-subject associationsfor a range of receptive (spoken word, written word,picture and sound comprehension) and expressivetasks (naming, verbal definitions, object use,drawing to name, and delayed copying). The

present data replicate these item associationsrepeatedly over time (for naming, object use,drawing, and verbal definitions) whilst extendingthe domains to include tactile naming. Theseresults support the notion that patients withsemantic dementia have a progressive impairmentto an amodal semantic system. They are not consis-tent with models of semantic memory that positseparate subsystems for verbal and visual modalities(e.g., McCarthy & Warrington, 1988; Shallice,1988). Under these schemes, there is no necessaryrelationship between the decline observed forverbal and nonverbal semantic performance.

The differences between verbal output (namingand definition) and nonverbal performance (objectuse and miming) could be taken as evidence infavour of a multiple semantic systems theory.Under that scheme, poor verbal performance arisesfrom a specific impairment to the verbal semanticsystem (cf. Lauro-Grotto et al., 1997). It is alsopossible to explain the same results if one assumesthat the patients have a combination of centralsemantic impairment and a deficit within the verbaldomain. There are, however, at least two differ-ences between object use and naming, which iftaken into account make the disparity betweennaming and object use consistent with the amodalsemantics hypothesis. As noted in the Introduc-tion, the mappings of semantics-to-phonology(cf. naming) and semantics-to-object structure (cf.object use) are different. The relationship betweensemantics and phonology is arbitrary whereas thesemantics-structure mapping is at least partiallysystematic: Elements within an object’s structureare associated with knowledge about that item and,in turn, how the object is used. These differenceshave been highlighted previously in explanations ofpoor verbal performance in patients with semanticimpairments (Caramazza et al., 1990; Rapp et al.,1993). When these alternative mappings areimplemented in PDP simulations, the modelsdemonstrate that semantic activation is moreaccurate for systematic than arbitrary mappings(Lambon Ralph & Howard, 2000; Plaut, 1999;Rogers et al., in press). This means that objectuse and naming performance will automaticallybe different for the same degree of underlying

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semantic impairment. Even a small semanticimpairment leads to a significant degree of anomia(Lambon Ralph et al., 2001) whereas the quasi-systematic mapping should produce better objectuse.

A second factor also benefits object use. Innearly all models of speech production, there is onlyone route from input (semantic memory) to output(speech). For object use, there are potentially tworoutes from vision to action: one via conceptualknowledge and the other representing affordances:that is, direct translations between vision andpraxis. These two routes may correspond to thedistinction between ventral and dorsal visualpathways, which can be differentially affected invarious neurological conditions (Hodges et al.,1999; Milner & Goodale, 1995). The distinctionbetween general semantic information and praxicknowledge has been demonstrated in other studies(Buxbaum & Saffran, 2002). In addition, a previousstudy with semantic dementia patients attemptedto specify affordances a priori and to test for theirinfluence on object use (Bozeat et al., 2002b). Thisinvestigation found that afforded elements ofobject use (e.g., gripping the handle of a hammer)were relatively preserved even in patients withsevere semantic impairment, supporting the notionof an independent route to action for these specific,limited aspects of object use. In patients withsemantic dementia, therefore, there are two formsof constraint on their object use—their remainingsemantic knowledge about objects plus affordances.Overall, this means that naming is only supportedby an arbitrary mapping from conceptual knowl-edge while object use benefits from a quasi-system-atic mapping from semantics in addition to aseparate form of constraint (affordances). Viewedin this way, it is unsurprising that object use isconsistently better than object naming.

Perhaps the most striking factor in this studywas the finding that both patients’ namingimproved dramatically when they were demon-strating or miming the use of objects rather thannaming in isolation (from vision or touch). At facevalue, this might appear to be inconsistent with anaccount based on a unitary semantic system. In bothcases, the same object was presented to the patient

and thus an identical naming outcome might havebeen expected. This assumes, however, that exactlythe same semantic information is activated in thetwo situations. As noted above, a number oftheories assume that semantic representations aredynamic in nature such that the form of informa-tion activated varies across modalities and contexts(Rapp et al., 1993). This effect was demonstrated ina previous study: Lambon Ralph and Howard(2000) found that IW, a patient with semanticdementia, was consistently worse when semanticswere required to interact with verbal representa-tions than when activated by pictures. Importantly,although certain meanings seemed to be consis-tently unavailable to IW from verbal-only input,her comprehension for these items improved whenthe words were presented with a picture context(semantically related to the target word). Thisresult shows that even degraded semantic represen-tations are dynamic: The poor semantic activationfrom verbal input was improved by a semanticallyrelated picture context. Lambon Ralph andHoward were also able to demonstrate the sameeffect in a PDP simulation: Verbal input was muchmore effective if the semantic system was first acti-vated by a pictorial input (even one that is onlyapproximately semantically related). This simula-tion provides a computational account of dynamicsemantic representations. Visual presentation acti-vates semantics more accurately than verbal inputbecause of the difference in mapping (see also Rappet al., 1993). When the two inputs are combined,the picture context activates a partially correctsemantic representation. This provides a betterstarting point for verbal input and, under thiscircumstance, words become more effective inactivating the specific target representation.

This account can be extended to explain howobject use might facilitate object naming. Theinitial visual presentation of the object activates apartially degraded semantic representation. Asthere is an arbitrary mapping with phonology, thisimpoverished conceptual knowledge is typicallyinsufficient to drive successful speech productionand the patient is unable to name the object. Thecombination of partially degraded semantics inconjunction with object affordances (direct visual-

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to-motor translations) means that, in the earlyphases of semantic dementia, object use is typicallypreserved. In computational frameworks, semanticmemory is represented within a fully interactivesystem (Lambon Ralph & Howard, 2000; Plaut,1999; Rogers et al., in press). This means that allaspects of correct object use (sensorimotor/kinaesthetic information from visual, tactile, andaction domains) will provide positive feedback tothe amodal semantic system. It is easy to imagine,therefore, that for relatively familiar objects, theimproved semantic activation is sufficient to kick-start speech production. Over time, as semanticrepresentations degrade further, all forms of output(naming, use, and naming during use) declinebecause they all rely on the same single, amodalsemantic system.

In conclusion, the longitudinal, cross-modalitydata of Elvezio and Dirce, together with those ofother patients with semantic impairment (Hillis etal., 1990; Lambon Ralph & Howard, 2000), high-light three key characteristics of conceptual knowl-edge and its breakdown in patients with semanticdementia: semantic representations are amodal; themapping between surface form and meaning variesfor different modalities; and the representations aredynamic.

Manuscript received 3 October 2002Revised manuscript received 24 March 2003

Revised manuscript accepted 7 May 2003

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