Unitary attention in callosal agenesis

UNITARY ATTENTION IN CALLOSAL AGENESIS

R. Dell’AcquaUniversity of Padova, Italy

P. Jolicoeur and M. LassondeUniversity of Montreal, Canada

A. AngrilliUniversity of Padova, Italy

P. De BastianiUniversity of Ferrara, Italy

A. PascaliUniversity of Padova, Italy

The interhemispheric organisation of two specific components of attention was investigated in threepatients affected by partial or complete agenesis of the corpus callosum. A visuospatial component ofattention was explored using a visual search paradigm in which target and distractors were displayedeither unilaterally within a single visual hemifield, or bilaterally across both visual hemifields in lightof prior work indicating that split-brain patients were twice as fast to scan bilateral displays comparedto unilateral displays. A central component of attention was explored using a psychological refractoryperiod (PRP) paradigm in which two visual stimuli were presented laterally at various stimulus onsetasynchronies (SOAs), with each stimulus associated with a different speeded two-alternative choicetask. The stimulus–response compatibility in the second task was systematically manipulated in thisparadigm, in light of prior work indicating that split-brain patients exhibited a close-to-normal PRPeffect (i.e., slowing of the second response as SOA is decreased), with, however, abnormally decreas-ing effects of the manipulation of the response mapping on the second task speed as SOA wasdecreased. The present results showed that, although generally slower than normals in carryingout the two tasks, the performance of each of the three acallosal patients was formally equivalentto the performance of a matched control group of normal individuals. In the visual search task,the search rate of the acallosal patients was the same for unilateral and bilateral displays.Furthermore, in the PRP task, there was more mutual interference between the lateralised tasksfor the acallosal patients than that evidenced in the performance of the matched control group. Itis concluded that the visuospatial component and the central component of attention in agenesisof the corpus callosum are interhemispherically integrated systems.

Correspondence should be addressed to Roberto Dell’Acqua, Department of Developmental Psychology, Via Venezia 8, 35131

Padova, Italy (Email: [email protected]).

This work was supported by grants from the Italian Ministry of Scientific Research (FIRB RBAU01LE9P) and the University of

Ferrara to RDA, and by research grants from the Natural Sciences and Engineering Research Council of Canada awarded to

ML and PJ.

COGNITIVE NEUROPSYCHOLOGY, 2005, 22 (8), 1035–1053

# 2005 Psychology Press Ltd 1035http://www.tandf.co.uk/journals/pp/02643294.html DOI:10.1080/02643290442000491

INTRODUCTION

The disconnection of the cerebral hemispheresprovides neuroscientists with the unique opportu-nity to study the cortical organisation of mentalprocesses in humans under conditions in whichthe bandwidth of information transfer betweenthe hemispheres is limited. Insights into theorganisation of mental processes have beenachieved in this context by channelling lateralisedstimulation to each disconnected hemisphere andmonitoring if and how the contralateral hemi-sphere can process the stimulation. Techniquesbased on lateralised stimulus presentationshave been used extensively to study the cerebralorganisation of functions in two specific popu-lations of neurological patients characterisedby disconnected cerebral hemispheres, namely,patients who have undergone surgical transectionof the corpus callosum (so-called split-brains;Sperry, 1968) and individuals affected by congeni-tal agenesis of the corpus callosum (or acallosals;e.g., Lassonde & Jeeves, 1994).

According to Sperry (1968), at least twointerdependent factors converge to establish abasic neurophysiological distinction in the cerebralcircuitry of split-brains and acallosals. In themajority of cases, the surgical transection of thecorpus callosum in split-brains is carried out inadulthood (usually, for treatment of intractableepilepsy), when the degree of neural plasticity ishypothesised to be reduced compared to earlierstages of development. Support for this view hascome from studies showing effective compen-sation for transection of the corpus callosum inparticipants who have undergone callosal surgerybefore puberty but poor compensation when theoperation was performed after puberty (e.g.,Lassonde, Sauerwein, Geoffroy, & Decarie,1986). Hypotheses concerning the functionalcompensation for the absence of the corpus callo-sum in acallosals have concentrated on the likelyhyper-development of uncrossed sensory-motorpathways, and on the enhanced transmission ofinformation through noncallosal or midbrain con-nections (e.g., Jeeves, 1994). Neuropsychologists

have demonstrated substantial differences betweensplit-brains and acallosals, using lateralised stimu-lus presentation techniques, primarily for threeaspects of cognitive performance (Lassonde &Jeeves, 1994). First, unlike split-brains, acallosalscan cross-match objects held in each hand out ofview. Second, acallosals do not seem to experienceany particular difficulty in cross-comparing tachis-toscopically presented visual stimuli. Finally,acallosals do not report hemialexia for wordschannelled to the right cerebral hemisphere, nordo they report anomia for real-world stimulihaptically explored using the left hand.

Despite the massive reorganisation of brainstructures that is arguably consequent to callosalagenesis, however, deficits of interhemispherictransfer of information in acallosals analogous tothe disconnection deficits typically shown bysplit-brains have been documented. Probablythe most compelling demonstration of defectiveinterhemispheric transfer in callosal agenesis isthat related to the crossed-uncrossed difference(CUD; Poffenberger, 1912) in speeded manualreaction time (RT) to lateralised visual stimuli.The CUD is hypothesised to estimate interhemi-spheric transmission time. This estimate has beenshown to be in the order of 3 or 4 ms in normals,and in the order of 50 ms or longer in split-brains.Interestingly, the CUD in acallosal patients iscloser in magnitude to that of split-brains thanto that of normals (e.g., Aglioti, Berlucchi,Pallini, Rossi, & Tassinari, 1993). An additionaldemonstration of the notable similarity betweensplit-brains and acallosal patients has beenreported in a study by Jeeves, Silver, andJacobson (1988). Like split-brains, acallosalpatients tend to fail in tasks requiring the inter-hemispheric integration of movements of theupper limbs under conditions in which such move-ments must be coordinated (see also Sauerwein,Lassonde, Cardu, & Geoffroy, 1981). A numberof studies have revealed acallosals’ deficits alsoto be comparable to split-brains’ deficits whenmotor learning skills mastered intrahemispheri-cally must be transferred interhemispherically,using either complex tactile stimuli, such as

DELL’ACQUA ET AL.

1036 COGNITIVE NEUROPSYCHOLOGY, 2005, 22 (8)

formboards or kinaesthetic mazes (see, amongothers, Jeeves, 1979), or simple visual stimuli(Lassonde, Sauerwein, & Lepore, 1995).

In contrast with the many studies reviewedabove, much less is known about the neural basisof attention in callosal agenesis. Only one studyhas focused on this issue and found that attentionin acallosal patients is similar to that found insplit-brains. Specifically, Hines, Paul, and Brown(2002) cued the location of an upcoming target.The cue was either valid, in that it accurately pre-dicted the location of the target, or it was invalid,in that it predicted another location. Acallosalpatients had greater difficulty than normal con-trols in reorienting attention to an invalidly cuedtarget when the cue and the target were displayedin opposite visual hemifields. Such difficultywas not apparent when the invalidly cued targetand the cue were displayed in the same visualhemifield. Notably, this pattern of resultsresembles that found with split-brains (Corballis,1995; Gazzaniga, 2000), and suggests that thecorpus callosum may be necessary to support anintegrated visuospatial attention system thatcrosses the vertical meridian.

In the present article, we seek to extend thework of Hines et al. (2002) by studying the char-acteristics of attentional performance in callosalagenesis using tasks designed to reveal differentaspects of the attention system of acallosals.These two tasks were the visual search and thepsychological refractory period (PRP) tasks.Whereas some work has been performed witheach of these tasks with split-brains, no equivalentwork has been done with acallosals.

In the visual search task, an observer must scana visual display, as rapidly as possible, to determinewhether a target is present or absent. Usually, thenumber of nontargets (distractors) in the display isvaried. If the target and distractors are structurallysimilar (e.g., a green “H” target among green “A”distractors), the search time increases linearly asthe number of distractors is increased (e.g.,Duncan & Humphreys, 1989; Treisman &Gelade, 1980). Luck, Hillyard, Mangun, andGazzaniga (1989, 1994) studied how split-brainssearch for a target in this type of task, with the

distractors surrounding the target either distribu-ted evenly in both visual hemifields, or confinedto a single hemifield. Strikingly, the search timeof split-brains was halved when distractors weredisplayed in both hemifields compared to whenthe stimuli were all in a single hemifield. Thatis, the search time of split-brains depended onthe number of items within each hemifieldrather than on the total number of distractors inthe entire visual field (both hemifields), as is typi-cally found with normal observers. These resultssuggest that independent visuospatial attentionmechanisms co-exist in the separate cerebralhemispheres of split-brains—is the same true foracallosals?

In the PRP task, two visual stimuli are pre-sented at various stimulus onset asynchronies(SOAs), typically ranging from 50 ms to 1000 msor longer. Each stimulus is associated with adifferent speeded task, and the reaction time(RT) in each task is recorded in each trial.Usually, RTs in the first task are not stronglyinfluenced by SOA. In contrast, RTs in thesecond task increase sharply as the SOA betweenthe stimuli is reduced. This is the PRP effect.Using lateralised stimuli, Pashler et al. (1994)presented split-brains with two sequential visualstimuli, one stimulus to the right of fixation andone stimulus to the left of fixation, each requiringa speeded binary decision. Like in normals, robustPRP effects were found in split-brains, suggestingthat whereas a visuospatial attention componentis not a unitary system in split-brains, a latercomponent of attention could not be dividedbetween two successive stimuli requiring inde-pendent speeded responses. However, using aparadigm similar to that used by Pashler et al.,Ivry, Franz, Kingstone, and Johnston (1998)argued that the locus of the PRP effect innormals and in split-brains differ substantially.Ivry et al. manipulated the spatial compatibilityof the stimulus–response mapping in the secondtask. A single split-brain case was examined inthis work. The split-brain tested and controlswere required to respond to a lateralised coloreddisk presented either above or below the hori-zontal meridian of a computer monitor using two

ATTENTION IN CALLOSAL AGENESIS

COGNITIVE NEUROPSYCHOLOGY, 2005, 22 (8) 1037

distinct stimulus–response mappings, namely,a “compatible” mapping (i.e., they pressed theupper button of two vertically aligned buttons toindicate that the disk was above the meridian,and the lower button to indicate that the diskwas below the meridian), or the inverse, “incom-patible” mapping. Not surprisingly, longer RTsin the second task were observed with the incom-patible mapping compared to the compatiblemapping. Of greater relevance, this spatial com-patibility effect was generally additive with thePRP effect in normal participants, but underaddi-tive in the split-brain (i.e., the spatial compatibil-ity effect decreased as SOA was decreased). Spatialcompatibility effects are held to emerge from alonger processing time required for response selec-tion when the response mapping is incompatible.In this context, the underadditive effects of SOAand spatial compatibility in the split-brain havebeen taken by Ivry et al. to indicate that each oftwo functionally independent central attentionmechanisms is likely to perform response selec-tion, and that these mechanisms coexist in the cer-ebral hemispheres of split-brains. The results ofIvry et al. were consistent with a locus of interfer-ence causing the PRP effect that, unlike innormals, was beyond response selection, at leastin the specific case of the split-brain tested in hisinvestigation. Do acallosals show the same appar-ent ability to carry out two independent responseselection operations, one in each hemisphere, assplit-brains?

Using the method devised by Luck et al. (1989,1994) and a variant of the PRP task close to Ivryet al.’s (1998), we examined visual search per-formance (Experiment 1) and PRP performance(Experiment 2) in three acallosals. These threeindividuals represented three distinct pointsalong the spectrum of callosal agenesis in termsof the degree of preservation of connectionslinking the two hemispheres. Patient A had anincomplete callosal agenesis with sparing of therostrum and the anterior commissure. Thispatient was presumably the least likely to have aperformance similar to that of split-brains. Atthe other extreme, Patient C had complete callosalagenesis and agenesis of the anterior commissure.

Finally, Patient B represented an intermediatecase, having complete callosal agenesis but anintact anterior commissure.

EXPERIMENT 1 (VISUALSEARCH TASK)

Method

ParticipantsPatient A is a 40-year old, right-handed male,with 5 years of formal education and an IQ of89. Callosal agenesis in this patient was first diag-nosed when he was 33 years old, after his recoveryfor an episode of hemicrania. According to MRI(top scan of Figure 1), the agenesis extends fromthe genu to the splenium of the corpus callosumwith sparing of the rostrum and the anterior com-missure. The disorder was classified in origin as aShapiro syndrome, due to some episodes of exces-sive sweating and disorders in thermoregulation,and treated with clozapine and clonazepam.However, such episodes have always been irregularand infrequent. In the last 7 years, on severaloccasions he has undergone in-depth neurologicalexamination. In none of these occasions haveneurological deficits been discovered. Thepatient was not on medication during the testingdescribed in the present article.

Patient B is a 32-year-old, left-handed manwith 6 years of formal education and an IQ of75. He started to have absence seizures at theage of 23 years following the installation of aventroperitoneal derivation for hydrocephaly. AnMRI (middle scan in Figure 1) performed atthat time revealed complete absence of thecorpus callosum with presence of the anteriorcommissure. The patient has been seizure-freefor several years and does not take any medication.His neurological exam is within normal limits.Patient B lives by himself and is gainfullyemployed.

Patient C is a 31-year-old, right-handed manwith 14 years of formal education and an IQ of107. He was born with various craniofacialmalformations such as hypertelorism, cleft lip,

DELL’ACQUA ET AL.


and cleft palate, which were surgically corrected atthe age of 4 months. In addition, a basal transpa-latal encephalocele was removed through a bifron-tal craniotomy at the age of 18 months. At thattime, complete agenesis of the corpus callosumwas detected. A subsequent MRI (bottom scanin Figure 1) also showed agenesis of the anteriorcommissure and discrete bilateral prefrontalatrophy related to the previous surgery. A lefthydrocele and two prepalatal fistulas, diagnosedat the age of 4 years, were also surgically corrected.As a consequence of the frontal surgery, he devel-oped hypothyroidism and hypopituitarism, whichresponded well to hormone therapy. He was noton medication at the time of testing. The patienthas a normal neurological exam. He is marriedand gainfully employed.

The control participants were five healthyadults. They were matched to the acallosals onthe basis of age, sex, and education, using thelowest level of education of the three acallosalsas the point of reference (5 years).

Patient A and the controls were tested at theNeuropsychological Lab of the S. Anna Hospitalin Ferrara, Italy, whereas patients B and C wereexamined at the Laboratory of the Groupe deRecherche en Neuropsychologie et Cognition ofthe University of Montreal, Canada.

Apparatus and stimuliA schematic representation of the spatial configur-ation of the stimuli on a trial of Experiment 1 isreported in Figure 2 (upper panel).

The display consisted of 2, 4, or 8 items, eachcomposed of a red square above or below a greensquare to form a vertically oriented rectangle sub-tending 0.88 � 0.48 at a distance of 50 cm set by achin-rest. The stimuli were displayed on a blackbackground of a CRT computer monitor con-trolled by a PC-type computer. Nontarget itemswere red-above-green rectangles, and targetitems were green-above-red rectangles. The itemswere placed at random locations within either orboth of two vertically oriented rectangularregions subtending 48 � 88, each centred 48 tothe left or to the right of a central fixation point

Figure 1. Magnetic resonance imaging scans (saggitalview) of acallosals. From top to bottom, patient A whohas a near-complete callosal agenesis but preservation ofthe rostrum and anterior commissure, Patient B who hasa complete callosal agenesis with an intact anteriorcommissure, and patient C, with agenesis of both thecallosal and anterior commissures.



Figure 2. Examples of the spatial configuration of the stimuli used in the visual search task (Experiment 1; upper panel) andin the PRP task (Experiment 2; lower panel).

DELL’ACQUA ET AL.


marked by a plus sign. In half of the trials, theitems were confined to a single hemifield (equallyoften left and right). In the other half of the trials,the stimuli were equally divided between the twohemifields. Half of each type of trial contained atarget (target-present trials) and half containedonly distractors (target-absent trials). Only onetarget was presented in any given target-presenttrial.

Control for eye movementsThe algorithm adopted for the control of eyemovements differed between the two settings(Italy and Canada). For Patient A and for eachof the adults included in the control group, hori-zontal eye movements were detected throughthree Ag/AgCl electrodes. Two electrodes wereplaced on the left and right lateral canthii, and aground electrode was placed in the centre of theforehead. The EOG was amplified using aColbourn amplifier, whose gain and band-passfilter were set to 5000 and 0.016–100 Hz, respect-ively. The EOG was sampled at 400 Hz by meansof a National Instruments 12-bit DAQCard-1200card. Before the beginning of the experimentalsession, each participant performed in an eyecalibration phase consisting of 30 eye movements(15 to the left and 15 to the right) from thecentral fixation point to the centre of the rectangu-lar regions (i.e., 48), within which stimuli werelater presented (see Figure 2). This distance waschosen because of the inherent low signal-to-noise ratio of the single-trial EOG recordedwith the present apparatus, and because only vari-ations in the EOG clearly exceeding 12 microV(i.e., 28) could be related with confidence to theproduction of an eye movement. Each participantalso made 30 analogous eye movements from thecentral fixation point to the outer boundary of thetwo rectangular regions (i.e., 68). Measurementsobtained during the calibration phase were usedto establish an EOG amplitude threshold for eyemovements of 48 or greater. For each trial, anEOG epoch of 1000 ms post-stimulus was selectedand the mean EOG amplitude recorded 250 mspre-stimulus (baseline) was subtracted. Following

the display onset in each trial, the latency of thefirst eye movement exceeding the threshold wasthen computed.

For patients B and C, lateral eye movementswere monitored during each trial by means ofa video camera (VHS AG-190 Panasonic) con-nected to a colour video monitor (Sony TrinitronPMV-1910Q). The camera was centred on oneof the patient’s eyes that covered the entiremonitor. A set of grid lines (1 cm ¼ 18) overlayedon the video monitor allowed the experimenter todetect any movements of the eyes. A central doton the grid indicated the eye position when theparticipant looked at the fixation point. Any trialin which there was eye movement prior to theresponse were flagged by the experimenter andlater excluded from statistical analyses of the data.The rejection criterion was quite severe; absolutelyno deviation of the eyes was allowed duringstimulus presentation.

ProcedureEach participant participated in four experimentalsessions, scheduled on two different days with twoconsecutive sessions per day. Each trial began withthe presentation of a fixation point displayed at thecentre of the monitor. The fixation point wasexposed for 1000 ms, and followed by a blankfield exposed for 800 ms. At the end of theblank field exposure, the items were displayed onthe monitor for a maximum duration of2500 ms. In the two sessions on one day, partici-pants were instructed to press one button withthe index finger of the right hand on target-present trials, or a different button with theindex finger of the left hand on target-absenttrials. In the other two sessions on the differentday, this response mapping was reversed. Theacallosals and three control participants startedwith two sessions in which right-hand responseshad to be produced on target-present trials, andleft-hand responses had to be produced ontarget-absent trials, followed by two sessionswith the other hand–response pairings. Twocontrol participants began with left-handresponses on target-present trials, and right-hand



responses on target-absent trials, followed by twosessions with the other pairings. Both speed andaccuracy were emphasised at the beginning ofeach session. A blank field was presented for2000 ms after the participant made a response,following which the fixation point for the nexttrial was presented. The fixation point providedfeedback on response accuracy. A plus sign indi-cated a correct response and a minus sign indicatedan error. Each session was divided into eightblocks of 24 trials each. The trials in one blockwere a randomised cycle through each possiblefactorial combination of the levels of number ofitems in the display (set size: 2, 4, or 8), spatiallayout (unilateral or bilateral), target presence/absence, unilateral display hemifield (left orright). Each participant contributed 768 exper-imental responses. The first session on each daywas preceded by a training phase composed oftwo blocks of 24 trials each.

Results

Only trials in which the target was displayed in thehemifield ipsilateral to the hand used for target-present responses were considered in the analyses.These trials were screened for eye movements, andonly trials free of eye movements were consideredin the analyses. Eye movement filtering resulted inthe loss of 17.3% of the acallosals’ trials, and 16.1%of the trials in the control group. The analysesconcentrated on correct RTs and error rates.Correct RTs were screened for outliers using anadaptation of the procedure described by VanSelst and Jolicoeur (1994). When an outlier oran error was found, the entire trial was excludedfrom the analyses. The application of the outlierelimination procedure on the present data setresulted in a loss of 3.0% of correct RTs for theacallosals, and 2.0% of correct RTs for thecontrol participants. The results were analysedusing an analysis of variance (ANOVA), inwhich set size (2 vs 4 vs 8 visual items) andspatial layout (unilateral vs. bilateral) weretreated as within-participant factors. In the separ-ate single-case analyses of the acallosals, session(total ¼ 4) was treated as random factor.

Control groupA graphical summary of the results of the controlgroup in Experiment 1 is reported in Figure 3(right lower panel). The RT analysis indicated asignificant effect of set size, F(2, 8) ¼ 20.8,MSe ¼ 7573, p , .001, and no effect of spatiallayout (F , 1), or of the interaction between setsize and spatial layout (F , 1). The analysisperformed on the mean percentage of correctresponses revealed a significant effect of set size,F(2, 8) ¼ 9.4, MSe ¼ 0.0087, p , .008, inwhich the percentage of correct responses tendedto decrease (from 95% to 78%) as set size increased.It also revealed a significant effect of thespatial layout. F(1, 4) ¼ 36.3, MSe ¼ 0.0019,p , .004, indicating a slightly higher accuracy ofthe control group with bilateral arrays than withunilateral arrays (91% vs 83%, respectively).Neither the effect of the spatial layout, nor theeffect of the interaction between set size andspatial layout, were significant in this analysis(both Fs , 1). The analyses performed on theparameters of the best-fitting linear regressionequations indicated that neither the slopes northe intercepts of unilateral vs bilateral linearequations differed significantly: slope, F , 1;intercept, F(1, 4) ¼ 2.8, MSe ¼ 63, p . .10.

Patients’ groupThe results obtained by each of the three acallosalpatients are also displayed in Figure 2. From theoutset, it can be seen that all three patientsshowed longer RTs than the controls. A detailedanalysis of each patient’s performance is presentedbelow.

Patient A (partial callosal agenesis, intact rostrum,and anterior commissure). A graphical summaryof the RT results of Patient A in Experiment 1is reported in Figure 3 (upper left panel). TheANOVA for the RT results indicated a significanteffect of set size, F(2, 6) ¼ 11.3, MSe ¼ 34144,p , .009, but no effect of the spatial layout(F , 1), and no interaction between set sizeand spatial layout (F , 1). The analysis per-formed on the mean percentage of correct

DELL’ACQUA ET AL.


responses revealed a marginally significant effectof set size, F(2, 6) ¼ 4.9, MSe ¼ 0.005, p , .06,reflecting a trend for the percentage of correctresponses to decrease (from 98% to 89%) as setsize increased. Neither the effect of spatiallayout, nor the effect of the interaction betweenset size and spatial layout, were significant inthis analysis (both Fs , 1). An analysis was alsoperformed on the parameters (i.e., slope andintercept) of the best-fitting linear regressionequations describing the RT functions associatedwith the unilateral and bilateral spatial layouts.These analyses indicated that neither the slopesnor the intercepts of the two linear equationsdiffered significantly: slope, F , 1; intercept,F(1, 3) ¼ 1.3, MSe ¼ 9606, p . .33.

Patient B (complete callosal agenesis, intact anteriorcommissure). A graphical summary of the RTresults of Patient B in Experiment 1 is reportedin Figure 3 (upper right panel). The ANOVAfor the RT results indicated a significant effectof set size, F(2, 6) ¼ 227.5, MSe ¼ 3093,p , .001, a significant effect of the spatiallayout, F(1, 3) ¼ 40.9, MSe ¼ 3651, p , .008,and no interaction between set size and spatiallayout, F(2, 6) ¼ 1.2, p . .33. The analysisperformed on the mean percentage of correctresponses revealed a significant effect of set size,F(2, 6) ¼ 24.1, MSe ¼ 0.003, p , .005, withthe percentage of correct responses decreasingfrom 94% to 80% as set size increased. Neitherthe effect of spatial layout, nor the effect of the

Figure 3. Visual search task RTs and standard error bars for the acallosals and the control group. The best-fitting linearequations for each RT function across set size are reported within the graphs (graphs are on different scales).



interaction between set size and the spatial layout,were significant in this analysis (both Fs , 1).The analysis performed on the parameters of thebest-fitting linear regression equations indicateda significant difference in slope between unilateraland bilateral RT functions, F(1, 3) ¼ 1399.6,MSe ¼ 0.85, p , .001 (note that this differenceis in the direction opposite than found forsplit-brains, as discussed below), and a signifi-cant difference in intercept between these func-tions, F(1, 3) ¼ 96.0, MSe ¼ 1542, p , .003.

Patient C (complete callosal agenesis, agenesis ofanterior commissure). A graphical summary ofthe RT results of Patient C in Experiment 1 isreported in Figure 3 (lower left panel). TheANOVA for the RT results indicated a marginallysignificant effect of set size, F(2, 6) ¼ 3.9,MSe ¼ 2074, p , .08, a significant effect of thespatial layout, F(1, 3) ¼ 19.2, MSe ¼ 2637,p , .03, and no interaction between set sizeand spatial layout, F(2, 6) ¼ 1.4, p . .32. Theanalysis performed on the mean percentage ofcorrect responses revealed a significant effect ofset size, F(2, 6) ¼ 32.7, MSe ¼ 0.005,p , .001, with the percentage of correct responsesdecreasing (from 89% to 64%) as set size increased.Neither the effect of spatial layout, nor the effect ofthe interaction between set size and the spatiallayout, were significant in this analysis, F , 1 andF(2, 6) ¼ 1.2, respectively, both ps . .40. Theanalysis performed on the parameters of thebest-fitting linear regression equations indicatedno significant difference in the slope of unilateraland bilateral RT functions, F(1, 3) ¼ 2.7,p . .2, and a significant difference in interceptbetween these functions, F(1, 3) ¼ 12.8,MSe ¼ 1780, p , .04.

Group analysesIn two separate ANOVAs, the group of acallosalswas compared directly with the control group. Inthis set of analyses, in addition to the factorsconsidered in the individual analyses, the factorgroup (acallosals vs controls) was considered as abetween-subject factor, and only effects relatedto this factor are discussed in this section.

Acallosals were generally slower than controls indetecting targets, F(1, 6) ¼ 7.7, MSe ¼ 208271,p , .04. No other effect involving the factorgroup emerged as significant in the RT analysis(all Fs , 1). No effects involving the factorgroup emerged as significant in the analysis ofaccuracy data (all Fs , 1).

Discussion

The most important results in Experiment 1 werethat the spatial layout of the items (unilateral vsbilateral) made either no difference to the rate ofvisual search for the acallosals and the controlgroup, or, when it did (Patients B and C), thepattern of RTs produced by this factor was notconvergent with the typical pattern shown bysplit-brains (i.e., search rate halved when scanninga bilateral display). In the case of Patient B, thesearch rate for bilateral displays was actuallyslower than the search rate for unilateral displays.In the case of Patient C, the search rate for bilat-eral displays was slower than for unilateraldisplays, but the difference between search rateswas minimal. Furthermore, in none of thesecases did the pattern of errors suggest an effectivemodulatory role of the spatial layout in the presenttask involving either the patients or the controlgroup. A comment concerning Patient C’s visualsearch performance is in order in the presentcontext. As is clear from Figure 3, Patient Cshowed search rates that were rather shallowcompared to the control group and the otherpatients. It is not entirely clear why this occurred.One indication might come from the particularlypronounced increase in errors for Patient C asset size increased, which might be suggestive ofa general predisposition of Patient C to tradespeed for accuracy on a larger proportion of trialscompared to the other participants tested.

EXPERIMENT 2 (PRP TASK)

Method

ParticipantsThe participants were the same as in Experiment 1.

DELL’ACQUA ET AL.


Apparatus and stimuliA schematic representation of the spatial configur-ation of the stimuli on a trial of Experiment 2 isshown in Figure 2 (lower panel). The visualstimuli were red or blue disks, with a diameter of1.08, displayed on the black background of thesame monitor as that used in Experiment 1. Oneach trial of Experiment 2, one red disk and oneblue disk were presented in succession, with thered disk 68 to the right of fixation and the bluedisk 68 to the left of two small fixation symbols(plus signs in Figure 2). Each disk could appear3.08 above or below the fixation location.

Control for eye movementsThe procedure and parameters for the control ofhorizontal eye movements were the same asthose used in Experiment 1. In the present exper-iment, two stimuli were presented sequentially oneach trial, and the latencies of the first two eyemovements following the onset of the first stimu-lus were computed, for control participants and forPatient A. For Patients B and C, the procedure foreye monitoring used in Experiment 1 was alsoused in the present experiment.

ProcedureEach participant participated in four experimentalsessions, scheduled on two different days with twosessions per day. Throughout an experimentalsession, participants rested the index and middlefingers of the left hand on the “Z” and “A” keysof the computer keyboard, and the index andmiddle fingers of the right hand on the “M” and“K” keys of the computer keyboard, respectively.These particular keys were selected because theslight tilt in the layout of “Z/A” and “K/M” keypairings on the computer keyboard assisted inmaking their correspondence with disk above/below the horizontal midline either spatiallycompatible (upper disk mapped to the upper key)or spatially incompatible (upper disk mapped tothe lower key).

Each trial began with the presentation of twofixation symbols displayed at the centre of

the monitor. The symbols were exposed for1000 ms, and followed by a blank field exposedfor 800 ms. At the end of the 800 ms blankfield, a first coloured disk was exposed for 80 mson one side of fixation, followed, after a stimulusonset asynchrony (SOA) of either 100, 340, or1000 ms, by a second coloured disk exposed for80 ms on the opposite side of fixation.Participants produced two independent responseson each trial, a first response to the first disk thatappeared, and a second response to the seconddisk, always using the hand ipsilateral to therespective disk. The fixation symbols also providedaccuracy feedback for the previous trial. The leftsymbol indicated accuracy of the first response,and the right symbol indicated accuracy of thesecond response. A plus sign signalled a correctresponse whereas a minus sign signalled an error.Each response had to be produced as quickly aspossible, while keeping errors to a minimum.The instructions emphasised both speed andaccuracy.

Each session was composed of two blocks of 48trials each, representing four randomised cyclesthrough each possible factorial combination ofthe levels of SOA (100, 340, or 1000 ms), spatialposition of first disk (above or below), andspatial position of the second disk (above orbelow). In the first block of trials of each of twoconsecutive sessions, participants were informedthat the first disk to appear was always the reddisk (right of fixation), followed by the blue disk(left of fixation). Participants pressed the “A” keywith the left middle finger if the red disk wasabove the horizontal meridian, or the “Z” key ifthe red disk was below the horizontal meridian.Participants then pressed the “K” key with theright middle finger if the blue disk was abovethe horizontal meridian, or the “M” key if theblue disk was below the horizontal meridian.The stimulus–response mapping for both disk inthis block of trials was spatially compatible, inthat the fingers closer to the body (i.e., the indexfingers) were mapped to disks appearing belowthe horizontal meridian, and fingers fartherfrom the body were mapped to disks appearingabove the horizontal meridian.



In the second block of trials within the samesession, the stimulus–response mapping for thefirst task remained constant whereas the stimulus–response mapping for the second task wasreversed, generating an incompatible mappingfor the second response. In this block, participantspressed the “K” key with the right middle finger ifthe blue disk was below the horizontal meridian,or the “M” key if the blue disk was above thehorizontal meridian. In each of the two other con-secutive sessions, the order of disks presentationwas reversed. Participants were informed thatthe first stimulus to appear was the blue disk tothe right of fixation, which was followed by thered disk to the left of fixation. In the first blockof trials within each of these sessions, participantsproduced a compatible response to each disk usingthe ipsilateral hands. In the other block of trials,the stimulus-response mapping for the secondtask was reversed. Thus, the first responsealways involved a compatible stimulus–responsemapping, whereas the second response couldeither involve a compatible or an incompatiblestimulus–response mapping. In this way, wemanipulated the compatibility of the stimulus–response mapping in Task 2 of the PRP paradigm(e.g., McCann & Johnston, 1992).

Patients A and C and two control participantsstarted with two sessions in which the red disk wasdisplayed first, followed by two sessions in whichthe blue disk was displayed first. Patient B andthe other two control participants started withtwo sessions in which the blue disk was displayedfirst, followed by two sessions in which the reddisk was displayed first. Each participant contrib-uted 384 responses to the first disk, and 384responses to the second disk. Each block of trialswas preceded by a practice block composed of 12trials resulting from one cycle through each poss-ible combination of the levels of SOAs, and spatialpositions of first and second disk.

Results

Trials were screened for eye movements, and onlytrials free of eye movements (for Patients A, B, C,and the control group) or trials in which the

latency of an eye movement was longer than therecorded RT in either task of the present paradigm(for Patient A and the control group only) wereconsidered in the analyses. Eye movement filter-ing resulted in the loss of 16.1% of the trialsfrom the acallosal patients, and 16.3% of thetrials from participants in the control group. Theanalyses concentrated on correct RTs and errorrates in each task. Correct RTs were screened foroutliers using the procedure used in Experiment1. When an outlier or an error was found ineither task, the entire trial was excluded fromfurther analysis. The outlier procedure rejected2.0% of correct RTs for the acallosals, and 2.2%of correct RTs for the control participants. Thescreened results were analysed using ANOVAs,in which SOA and Task 2 stimulus–responsemapping compatibility in the second task weretreated as within-participant factors. In the separ-ate single-case analyses of the acallosals, session(total ¼ 4) was treated as the random factor.

Task 1Control group. Figure 4 (lower right panel) showsthe RT performance of the control group. Task 1RTs are plotted using dashed lines. As can be seen,there was a significant effect of Task 2 mappingcompatibility, F(1, 4) ¼ 26.3, MSe ¼ 2276,p , .007. However, neither the effect of SOA,F(2, 8) ¼ 2.81, MSe ¼ 1479, p . .11, nor theinteraction between SOA and compatibility,F(2, 8) ¼ 2.2, MSe ¼ 820, p . .16, were sig-nificant. The mean percentage of correct responsesin Task 1 was 94%. None of the factors was signifi-cant (all Fs , 1) in an analysis performed on themean percentage of correct responses in Task 1.

Patient A (partial callosal agenesis, intact rostrum,and anterior commissure). Figure 4 (upper leftpanel) shows the RT performance of PatientA. Task 1 RTs are plotted using dashed lines.RTs increased slightly as SOA was reduced,F(2, 6) ¼ 23.8, MSe ¼ 2248, p , .002. Therewas also a significant effect of Task 2 mappingcompatibility, F(1, 3) ¼ 37.6, MSe ¼ 4663, p ,

.001. However, there was no interaction betweenthese two factors (F , 1). The mean percentage

DELL’ACQUA ET AL.


of correct responses in Task 1 was 88%. None ofthe factors was significant (all Fs, 1) in an analy-sis performed on this variable.

Patient B (complete callosal agenesis, intact anteriorcommissure). Figure 4 (upper right panel) showsthe RT performance of Patient B. Task 1 RTsare plotted using dashed lines. RTs tended toincrease as SOA was reduced, F(2, 6) ¼ 4.6,MSe ¼ 3589, p , .07. There was also a margin-ally significant effect of Task 2 mapping com-patibility, F(1, 3) ¼ 8.0, MSe ¼ 29641,p , .07. The interaction between these factorswas not significant, F(2, 6) ¼ 1.9, p . .22. Themean percentage of correct responses in Task 1was 89%. None of the factors was significant (allFs , 1) in an analysis performed on this variable.

Patient C (complete callosal agenesis and agenesisof anterior commissure). Figure 4 (lower leftpanel) shows the RT performance of Patient C.Task 1 RTs are plotted using dashed lines. RTsincreased as SOA was reduced, F(2, 6) ¼ 7.6,MSe ¼ 7733, p , .03. There was also a significanteffect of Task 2 mapping compatibility,F(1, 3) ¼ 270.6,MSe ¼ 812, p , .001, and a sig-nificant interaction between the two factors, F(2,6) ¼ 71.8,MSe ¼ 321, p , .001. The mean per-centage of correct responses in Task 1 was 88%. Theanalysis on this variable revealed a significanteffect of Task 2 mapping compatibility, F(1,3) ¼ 12.1, MSe ¼ 0.004, p , .05, with moreerrors when Task 2 mapping was incompatible(11%) than compatible (2%), and a significantinteractions between SOA and Task 2 mapping

Figure 4. PRP task RTs and standard error bars for the acallosals and the control group. Note that response–mappingcompatibility (compatible vs. incompatible) was manipulated in Task 2 only (graphs are on different scales).



compatibility, F(2, 6) ¼ 388.0, MSe ¼ 0.001,p , .001. There was a substantial trend of compat-ibility effects on accuracy to be particularly pro-nounced at long and short SOAs (12% and 11%,respectively) compared to the middle SOA (4%).

Task 2Control group. The mean RT in Task 2 is shownusing solid lines in the lower right panel ofFigure 4. As expected, RT increased as SOA wasreduced, F(2, 8) ¼ 111.2, MSe ¼ 1556,p , .001, and RT was longer for the incompati-ble mapping than for the compatible mapping,F(1, 4) ¼ 74.6, MSe ¼ 2809, p , .001.Furthermore, the effect of compatibility increasedas SOA was reduced, producing an overadditiveinteraction between compatibility and decreasingSOA, F(2, 8) ¼ 19.6, MSe ¼ 380, p , .001.The mean percentage of correct responses in Task2 was 92%. None of the factors was significant (allFs , 1) in an analysis performed on this variable.

Patient A (partial callosal agenesis, intact rostrumand anterior commissure). Task 2 RTs areplotted using solid lines in the upper left panelof Figure 4. The analysis revealed a significanteffect of SOA, F(2, 6) ¼ 499.0, MSe ¼ 1544,p , .001, a significant effect of Task 2 mappingcompatibility, F(1, 3) ¼ 674.1, MSe ¼ 2002,p , .001. There was also a significant interactionbetween these two factors, F(2, 6) ¼ 52.3,MSe ¼ 1665, p , .001, reflecting an increasein the effect of compatibility as SOA decreased(from 736 ms at the longest SOA to 1155 at theshortest SOA). The mean percentage of correctresponses in Task 2 was 93%. An analysis per-formed on this variable revealed a significant effectof Task 2 mapping compatibility, F(2, 6) ¼ 37.3,MSe ¼ 0.0003, p , .001, reflecting more errorswith the incompatible Task 2 mapping than withthe compatible Task 2 mapping (21% vs 3%,respectively). There was also a significant inter-action betweenSOAandTask 2mapping compati-bility, F(2, 6) ¼ 9.0, MSe ¼ 0.0009, p , .02,indicating an increase in the effect of Task 2mapping compatibility on errors as SOA decreased

(from 13% at the longest SOA to 26% at theshortest SOA).

Patient B (complete callosal agenesis, intact anteriorcommissure). Task 2 RTs are plotted using solidlines in the upper right panel of Figure 4. Theanalysis revealed a significant effect of SOA,F(2, 6) ¼ 44.4, MSe ¼ 12717, p , .001, a sig-nificant effect of Task 2 mapping compatibility,F(1, 3) ¼ 16.37, MSe ¼ 86940, p , .001, andno significant interaction between these factors,F(2, 6) ¼ 1.1, p . .4. The mean percentage ofcorrect responses in Task 2 was 93%. Ananalysis performed on this variable revealed asignificant effect of Task 2 mapping compatibility,F(2, 6) ¼ 37.3, MSe ¼ 0.0003, p , .001,reflecting more errors with the incompatibleTask 2 mapping than with the compatible Task2 mapping (2% vs 10%, respectively). SOA andthe interaction between SOA and Task 2mapping compatibility factors did not producesignificant effects (all Fs , 1).

Patient C (complete callosal agenesis, agenesis ofanterior commissure). Task 2 RTs are plottedusing solid lines in the lower left panel ofFigure 4. The analysis revealed a significanteffect of SOA, F(2, 6) ¼ 16.5, MSe ¼ 11522,p , .004, a significant effect of Task 2 mappingcompatibility, F(1, 3) ¼ 57.4, MSe ¼ 4591,p , .005, and a significant interaction betweenthese two factors, F(2, 6) ¼ 13.3, MSe ¼ 4992,p , .007, reflecting the evident oveadditive inter-action between Task 2 mapping compatibility anddecreasing SOA. The mean percentage of correctresponses in Task 2 was 92%. An analysisperformed on this variable revealed a marginallysignificant effect of Task 2 mapping compatibility,F(1, 3) ¼ 8.6, MSe ¼ 0.007, p , .07, reflectingthe trend of more errors with the incompatibleTask 2 mapping (11%) than with the compatibleTask 2 mapping (3%). SOA and the interac-tion between SOA and Task 2 mapping com-patibility did not produce significant effects,F(2, 6) ¼ 2.0, p . .21, and F(2, 6) ¼ 2.8,p . .15, respectively.

DELL’ACQUA ET AL.


Group analysesIn a set of separate ANOVAs, the group of acallo-sals was compared directly with the control group.In this set of analyses, in addition to the factorsconsidered in the individual analyses, the factorgroup (acallosals vs controls) was considered as abetween-subject factor, and only effects relatedto this factor are discussed in this section.Consider first the results for the first response.Acallosals were slower than controls in producingthe first response, F(1, 6) ¼ 30.8,MSe ¼ 33374,p , .01, and the SOA effect on RT1 was largerfor acallosals for controls, F(2, 12) ¼ 8.0,MSe ¼ 1518, p , .01. Furthermore, acallosalsshowed a greater compatibility effect (i.e., slowerRT1 for incompatible responses in Task 2) com-pared to controls, F(1, 6) ¼ 14.7, MSe ¼ 4317,p , .02.

Consider now the results for the second response.Acallosals were slower than controls, F(1,6) ¼ 14.4,MSe ¼ 199286, p , .01, and showeda greater PRP effect compared to controls, F(2,12) ¼ 10.4, MSe ¼ 5760, p , .01. There wasalso a three-way interaction involving group, SOA,and response compatibility, F(2, 12) ¼ 9.5,MSe ¼ 1255, p , .03. Although both groupstended to show an overadditive effect of compati-bility with decreasing SOA (i.e., greater com-patibility effects at short vs long SOA), thisinteractionwas larger for acallosals than for controls.The factor group did not produce significanteffects on Task 1 or Task 2 accuracy (all Fs , 1).

Discussion

The most important results of the presentexperiment were that none of the three acallosalsproduced underadditive effects of Task 2stimulus–response compatibility with decreasingSOA. One of them (Patient B) produced additiveeffects, whereas the other two (A, C) producedclearly overadditive effects. Results from thecontrol group were also overadditive, but to alesser degree on average. In contrast, Ivry et al.(1998) found that the effects of stimulus–responsecompatibility in Task 2 of a PRP experimentwere underadditive with decreasing SOA in a

split-brain, in contrast with an overadditiveeffect found with their control participants. Theresults from our acallosals were thus moresimilar to those of normal control participantsthan to those found with Ivry et al.’s split-brain.The underadditive effect found with the split-brain suggests that this patient was able tooverlap the mental operations required toperform the response selection in Task 2 concur-rently with those required to perform responseselection in Task 1 (see McCann & Johnston,1992; Pashler, 1994; Van Selst & Jolicoeur,1997). Like normal participants, the acallosalswere unable to perform response selection oper-ation in Task 2 in parallel with the concurrentresponse selection required to perform Task1. As such, the pattern of behaviour exhibited byall three acallosals was functionally more similarto that of normal controls than that of Ivryet al.’s split-brain.

We note that all three acallosals were morestrongly affected by the stimulus–response com-patibility manipulation than were the controlparticipants. Callosal agenesis is known to resultin a reduction of cortical cells that normallyreceive commissural input (Shoumura, Ando, &Kato, 1975). This in turn could alter the atten-tional control capacities of each hemisphere, thusleading to deficits in disengagement under theincompatible condition. Nevertheless, the factthat all three acallosals showed a pattern of beha-viour similar to that of the controls points to acoupling between the response selection oper-ations required to respond with each of the twohands. Again, this result is consistent with thehypothesis that there is a single central attentionalcontrol system—carrying out response selectionoperations under the present testing conditions—in acallosals, unlike what has been hypothesizedto be the case for the split-brain tested by Ivryet al. (1998).

GENERAL DISCUSSION

Recent developments in neuroscience suggest thatattention is not a unitary function of the brain



(e.g., Parasumaran, 1998). Rather, several neuro-physiological studies (some reviewed in Motter,1998) argue for a fractionation of attention intomultiple components, each engaging a finite setof cerebral circuits distributed across severalbrain loci. The present work examined two dis-tinct components of attention in three patientswith different forms of agenesis of the corpuscallosum, with and without presence of theanterior commissure. A visuospatial componentof attention was examined in Experiment 1using a variant of a visual search paradigm apt toprovide a direct estimate of the degree of func-tional independence of the cerebral hemispheresin scanning the visual field for the presence of aspecified target. A central component of attentionwas examined in Experiment 2 using a dual-task(psychological refractory period, PRP) paradigm,which has been hypothesised to reflect centralattention limitations (e.g., Jolicoeur, 1999;Pashler, 1994). Importantly for the present pur-poses, both these paradigms reveal disconnectionsymptoms when administered to commissuroto-mised, split-brain patients.

Each of the present experiments generatedresults that were clear-cut in showing no sign ofdisconnection symptoms in callosal agenesis. Inthe visual search paradigm, the reaction times(RTs) of acallosals and control participants weremodulated by the number of items displayed inthe visual field, independent of whether theitems were displayed unilaterally or bilaterally.This pattern is clearly different from what hasbeen observed in split-brains, for whom searchslopes decrease when items are displayed bilater-ally (Luck et al., 1989, 1994). The results ofExperiment 1 suggest a different picture of thecerebral organisation of the visuospatial attentionsystem in callosal agenesis than Hines et al.(2002) have advocated based on results obtainedwith a spatial cuing paradigm (see Introduction).Although the results of Hines et al. are congruentwith the principle that a callosum-mediated visualintegration process is demanded whenever thefocus of attention crosses the subjective verticalmeridian, the results of Experiment 1 supportthe notion that the visuospatial attention system

is interhemispherically integrated in the presentacallosals, conceivably by virtue of the subcorticalstructures that are preserved in these patients.The fact that one of our acallosals (C) alsolacked the anterior commissure suggests that thisstructure is not necessary for this type of inte-gration. The apparent incongruence between thepresent study and the study of Hines andcolleagues is all the more interesting in light ofprevious suggestions for a functional analogy ofthe attention mechanisms mediating visual searchand those mediating spatial shifts of attentioninduced by spatial cues (e.g., Luck & Girelli,1998). An analogy also exists at a neuroanatomicallevel between the brain areas involved in thesetasks. It has indeed been shown that posterior par-ietal areas play a major role in both visual searchand cuing tasks (Ashbridge, Walsh, & Cowey,1997), with the posterior part of the corpus callo-sum representing the specialised support for aninterhemispheric connection between these areas(e.g., Reuter-Lorenz & Fendrich, 1990).

Concerning the difference between the presentvisual search findings and the results reported inthe study by Hines and colleagues and mentionedin the Introduction, some have argued (e.g.,Lepore, Lassonde, Poirier, Schiavetto, &Villette, 1994) that the impairment described byHines and colleagues stems from a deficit inintegrating visual information in the proximityof the vertical meridian, namely, a problem dueto the small eccentricity of the stimuli acallosalshad to respond to. It is, however, important tonote that the difference between the Hines study(finding increased costs of invalid cross-fieldcueing in acallosals) and the present study cannotbe explained in terms of stimulus eccentricity. Thestimuli in the study by Hines et al. were centred3.58 left and right of fixation, which is a similardistance to the centre of the search fields in thepresent study (i.e., 48). This makes eccentricityunlikely to be a discriminant factor betweenthese studies. The difference between the Hineset al. study and the present work may rather bethat the invalid cueing condition in the spatialcueing experiments required stimulus-drivenreorienting of attention between hemifields,

DELL’ACQUA ET AL.


which was not (or less) required in the currentsearch task. Stimulus-driven reorienting (or“circuit breaking”) processes, involving thetemporoparietal junction area (Corbetta,Kincade, Ollinger, McAvoy, & Shulman, 2000;Friedrich, Egly, Rafal, & Beck, 1998), seem torely on an intact splenium (Pollmann, Maertens,& Von-Cramon, 2004). The Hines et al. datasuggest that acallosal patients may lack an efficientinterhemispheric pathway for these signals. Thetop-down controlled serial search processesrequired in the present visual search task, invol-ving rather superior parietal structures (e.g.,Muller, Donner, Bartelt, Brandt, Villringer, &Kleinschmidt, 2003), may instead be connectedvia subcortical commissures.1

In the PRP paradigm implementingthe manipulation of stimulus–response (SR)mapping compatibility in the second task(Experiment 2), both controls and the acallosalsshowed a substantial cross-talk between tasks, inthe form of an effect of the Task 2 manipulationon response times in Task 1. This in turn mayhave contributed to the overadditive interactionbetween the mapping manipulation and themanipulation of the degree of temporal overlap(i.e., stimulus onset asynchrony, SOA) betweenthe concurrent tasks. Ivry et al. (1998) haveshown that one split-brain observer exhibited arather different response pattern: In the secondtask of the PRP paradigm, they revealed aneffect of the mapping manipulation that wasunderadditive with decreasing SOA, suggestinga locus of dual-task interaction that was beyondresponse selection, possibly at a stage of motorinitiation required to maintain well-coordinatedmotor behaviour. Although it is quite possiblethat the lack of a known replication of Ivry’sfinding in the literature may weaken the con-clusions drawn from his study, which was basedon results obtained from a single split-brainpatient, the crucial evidence obtained in thepresent experimental context is suggestive ofmechanisms mediating the interaction between

response compatibility effects and SOA effects inacallosals that are interhemispherically connected.

The combined analyses of the results ofExperiments 1 and 2 revealed further importantdetails that may be critical in the interpretationof the present findings, and in the understandingof the cerebral organisation of attention processesin callosal agenesis. Namely, in Experiment 1, thesearch rate for the acallosals was lower than that ofcontrols, and there was a tendency of the interceptof the regression equation for the acallosals to bemore elevated than the intercept for controls. Inaddition, in Experiment 2, the size of themapping manipulation effect and the size of thePRP effect in the second task were both more pro-nounced in the acallosals than in the matchedcontrol group, as were also the overadditiveeffects of compatibility and SOA. Several studieshave indicated an increase in response times inacallosals during processing of visual stimuli pre-sented either intra- or interhemispherically (e.g.,Lassonde, 1994). These results have been inter-preted within the context of a facilitatory influenceexerted by the corpus callosum on perceptualprocessing. The present findings suggest thatthis interpretation may extend to attentionalcapacities. At the anatomical level, callosal agen-esis has been found to result in the loss of corticalcells that are normally receiving a callosal input(Shoumura et al., 1975). This loss of callosallyrecipient cells could in turn lead to reduced corti-cal activation, thus inducing central attentionallimitations. In this context, the important com-patibility effects observed in all three acallosalpatients may reflect greater deficits in attentiondisengagement.

The analogy between the overall patterns ofresults in acallosals and controls is entirely consist-ent with an organisation of visuospatial attentionsystems and of central-attention systems in acallo-sals that are functionally equivalent to those ofnormal controls, but that function less efficientlyin acallosals. The differences between theperformance of acallosals and that of split-brains

1 We are indebted to one anonymous reviewer for suggesting this insightful explanation of the difference between the results in

the present work and the work by Hines et al. (2002).



provide interesting contrasts and suggest that theabsence of the corpus callosum early in develop-ment does not prevent the elaboration of anormal organisation of attention subsystems. Incontrast, the loss of the corpus callosum later inlife, when brain plasticity is reduced, is morelikely to produce disruptions in attentional organ-isation. Although more work will be required todetermine whether the patterns of results wefound in these acallosals generalise to all cases ofcallosal agenesis, our results suggest that the struc-ture of the functional architecture of spatialattention and central attention can be normal(although perhaps less efficient) even in thecomplete absence of the corpus callosum and ofthe anterior commissure, provided the absence ofthese structures occurs early in development.

Manuscript received 15 September 2004

Revised manuscript received 13 December 2004

Revised manuscript accepted 25 January 2005

Preview proof published online 26 May 2005

REFERENCES

Aglioti, S., Berlucchi, G., Pallini, R., Rossi, G. F., &Tassinari, G. (1993). Hemispheric control of uni-lateral and bilateral responses to lateralized lightstimuli after callosotomy and in callosal agenesis.Experimental Brain Research, 95, 151–165.

Ashbridge, E., Walsh, V., & Cowey, A. (1997).Temporal aspects of visual search studied by tran-scranial magnetic stimulation. Neuropsychologia, 35,1121–1131.

Conti, F., & Manzoni, T. (1994). The neurotransmit-ters and postsynaptic action of callosally projectingneurons. Behavioural Brain Research, 64, 37–53.

Corballis, M. C. (1995). Visual integration in the splitbrain. Neuropsychologia, 33, 937–959.

Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy,M. P., & Shulman, G. L. (2000). Voluntary orient-ing is dissociated from target detection in humanposterior parietal cortex. Nature Neuroscience, 3,292–297.

Duncan, J., & Humphreys, G. W. (1989). Visual searchand stimulus similarity. Psychological Review, 96,433–458.

Friedrich, F. J., Egly, R., Rafal, R. D., & Beck, D.(1998). Spatial attention deficits in humans: A com-parison of superior parietal and temporo-parietaljunction lesions. Neuropsychology, 12, 193–207.

Gazzaniga, M. (2000). Cerebral specialization andinterhemispheric communication: Does the corpuscallosum enable the human condition? Brain, 123,1293–1326.

Hines, R. J., Paul, L. K., & Brown, W. S. (2002).Spatial attention in agenesis of the corpus callosum:Shifting attention between visual fields.Neuropsychologia, 40, 1804–1814.

Ivry, R. B., Franz, E. A., Kingstone, A., &Johnston, J. C. (1998). The psychological refractoryperiod effect following callosotomy: Uncoupling oflateralized response codes. Journal of ExperimentalPsychology: Human Perception and Performance, 24,463–480.

Jeeves, M. A. (1979). Some limits to interhemisphericintegration in cases of callosal agenesis and partialcommissurotomy. In I. S. Russel, M. W. van Hof,& G. Berlucchi (Eds.), Structure and function of

cerebral commissures (pp. 449–474). London:MacMillan Press.

Jeeves, M. A. (1994). Callosal agenesis—a natural splitbrain: Overview. In M. Lassonde & M. A. Jeeves(Eds.), Callosal agenesis—a natural split brain?

(pp. 285–299). New York: Plenum Press.Jeeves, M. A., Silver, P. H., & Jacobson, I. (1988).

Bimanual coordination in callosal agenesisand partial commissurotomy. Neuropsychologia, 26,833–850.

Jolicoeur, P. (1999). Dual-task interference andvisual encoding. Journal of Experimental

Psychology: Human Perception and Performance, 25,596–616.

Lassonde, M. (1994). The facilitatory influence of thecorpus callosum. In M. Lassonde & M. A. Jeeves(Eds.), Callosal agenesis—a natural split brain?

(pp. 275–284). New York: Plenum Press.Lassonde, M., & Jeeves, M. A. (1994). Callosal

agenesis—a natural split brain? New York: PlenumPress.

Lassonde, M., Sauerwein, H. C., & Lepore, F. (1995).Extent and limits of callosal plasticity: Presence ofdisconnection symptoms in callosal agenesis.Neuropsychologia, 33, 989–1007.

Lassonde, M., Sauerwein, H. C., Geoffroy, G., &Decarie, M. (1986). Effects of early and late transec-tion of the corpus callosum in children. Brain, 109,953–967.

DELL’ACQUA ET AL.


Lepore, F., Lassonde, M., Poirier, P., Schiavetto, A., &Villette, N. (1994). Midline sensory integration incallosal agenesis. In M. Lassonde & M. A. Jeeves(Eds). Callosal agenesis—a natural split brain?

(pp. 155–160). New York: Plenum Press.Luck, S. J., & Girelli, M. (1998). Electrophysiological

approaches to the study of selective attention inthe human brain. In R. Parasuraman (Ed). The

attentive brain (pp. 71–94). Cambridge, MA:MIT Press.

Luck, S. J., Hillyard, S. A., Mangun, G. R., &Gazzaniga, M. S. (1989). Independent hemisphericattentional systems mediate visual search in split-brain patients. Nature, 342, 543–545.

Luck, S. J., Hillyard, S. A., Mangun, G. R., &Gazzaniga, M. S. (1994). Independent attentionalscanning in the separated hemispheres of split-brain patients. Journal of Cognitive Neuroscience, 6,84–91.

McCann, R. S., & Johnston, J. C. (1992). Locus of thesingle-channel bottleneck in dual-task interference.Journal of Experimental Psychology: Human

Perception and Performance, 18, 471–484.Miller, J. (2004). Exaggerated redundancy gain in the

split brain: A hemispheric coactivation account.Cognitive Psychology, 49, 118–154.

Motter, B. C. (1998). Neurophysiology of visual atten-tion. In R. Parasuraman (Ed.), The attentive brain(pp. 51–70). Cambridge, MA: MIT Press.

Muller, N. G., Donner, T. H., Bartelt, O. A.,Brandt, S. A., Villringer, A., & Kleinschmidt, A.(2003). The functional neuroanatomy of visualconjunction search: A parametric fMRI study.Neuroimage, 20, 1578–1590.

Parasuraman, R. (1998). The attentive brain.

Cambridge, MA: MIT Press.Pashler, H. (1994). Dual-task interference in simple

tasks: Data and theory. Psychological Bulletin, 116,220–244.

Pashler, H., Luck, S. J., Hillyard, S. A., Mangun, G. R.,O’Brien, S., & Gazzaniga, M. S. (1994). Sequentialoperation of disconnected cerebral hemispheres insplit-brain patients. Neuroreport, 5, 2381–2384.

Poffenberger, A. T. (1912). Reaction time to retinalstimulation with special reference to the time lostin conduction through nervous centers. Archives ofPsychology, 23, 1–73.

Pollmann, S., Maertens, M., & Von-Cramon, D. Y.(2004). Splenial lesions lead to supramodal targetdetection deficits. Neuropsychology, 18, 710–718.

Posner, M. I., & Petersen, S. E. (1990). The attentionsystem of the human brain. Annual Review of

Neuroscience, 13, 25–42.Reuter-Lorenz, P. A., & Fendrich, R. (1990).

Orienting attention across the vertical meridian:Evidence from callosotomy patients. Journal of

Cognitive Neuroscience, 2, 232–238.Sauerwein, H. C., Lassonde, M., Cardu, B., &

Geoffroy, G. (1981). Interhemispheric integrationof sensory and motor functions in agenesis of thecorpus callosum. Neuropsychologia, 19, 445–454.

Shoumura, K., Ando, T., & Kato, K. (1975). Structuralorganization of callosal Obg in human corpuscallosum agenesis. Brain Research, 93, 241–252.

Sperry, R. W. (1968). Plasticity of neural maturation.Developmental Biology, 2 (suppl.), 306–327.

Treisman, A. M., & Gelade, G. (1980). A featureintegration theory of attention. Cognitive

Psychology, 12, 97–136.VanRullen, R., Reddy, L., & Koch, C. (2004). Visual

search and dual-tasks reveal two distinct attentionalresources. Journal of Cognitive Neuroscience, 16, 4–14.

Van Selst, M., & Jolicoeur, P. (1994). A solution to theeffect of sample size on outlier elimination.QuarterlyJournal of Experimental Psychology, 47A, 631–650.

Van Selst, M., & Jolicoeur, P. (1997). Decision andresponse in dual-task interference. Cognitive

Psychology, 33, 266–307.



Unitary attention in callosal agenesis

Documents

Transcript of Unitary attention in callosal agenesis