Functional MT + lesion impairs contralateral motion processing

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Functional MT + lesion impairs contralateralmotion processingLauren R. Moo a , Britt C. Emerton a b & Scott D. Slotnick ca Neuropsychology Laboratory, Department of Neurology , MassachusettsGeneral Hospital , Boston, MA, USAb Suffolk University , Boston, MA, USAc Psychology Department , Boston College , Chestnut Hill, MA, USAPublished online: 21 Aug 2008.

To cite this article: Lauren R. Moo , Britt C. Emerton & Scott D. Slotnick (2008) Functional MT +lesion impairs contralateral motion processing, Cognitive Neuropsychology, 25:5, 677-689, DOI:10.1080/02643290802271599

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Functional MT1 lesion impairscontralateral motion processing

Lauren R. MooNeuropsychology Laboratory, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA

Britt C. EmertonNeuropsychology Laboratory, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA, and Suffolk University, Boston,

MA, USA

Scott D. SlotnickPsychology Department, Boston College, Chestnut Hill, MA, USA

Human motion processing region MTþ is retinotopically organized with perception of and attentionto motion in the right visual field preferentially associated with left MTþ activity and vice versa.However, the degree towhichMTþ is crucial formotion processing is uncertain.We report an epilepsypatient with visual symptoms early in his seizure evolution and a left temporal-occipital seizure onsetelectrographically in whom we hypothesized a functional left MTþ lesion. The patient was impairedin his right but not left visual field on a hemifield motion attention task and demonstrated worse per-formance on a hemifield picture identification task when pictures implying motion were presented inthe right as opposed to the left visual field. FunctionalMRI (fMRI) during a full-fieldmotion detectiontask activated rightMTþ but failed to activate leftMTþ despite activating both left and rightMTþin each of 10 controls. Furthermore, fMRI during a hemifield motion attention task also showed a lackof leftMTþ attention effects in the patient. Together these results suggest thatMTþ is necessary fornormal motion processing.

Keywords: Functional magnetic resonance imaging; Vision; Epilepsy; Attention; Perception.

Feature-specific cortical processing regions havebeen identified in nonhuman primates and humans,including regions that preferentially process objectshape, colour, and motion. Such processing occursrelatively early in the visual cortical processingstream (Felleman & Van Essen, 1991), and this

information can be assumed to ultimately convergeto yield a unified object percept. In humans, theprocessing characteristics of these feature-specificregions are under active investigation.

The present article focuses on human motionprocessing region MTþ (the analogue of monkey

Correspondence should be addressed to Lauren R. Moo, Neuropsychology Laboratory, Department of Neurology,

Massachusetts General Hospital, 175 Cambridge Street, Suite 340, Boston, MA 02114, USA (E-mail: [email protected]).

This work was supported by Grant DC005068 from the National Institute for Deafness and Communication Disorders (to

L.R.M.).

# 2008 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business 677http://www.psypress.com/cogneuropsychology DOI:10.1080/02643290802271599

COGNITIVE NEUROPSYCHOLOGY, 2008, 25 (5), 677–689

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motion processing regions middle temporal, MT,and medial superior temporal, MST; Livingstone &Hubel, 1988; Van Essen & Gallant, 1994).Neuroimaging studies (employing positron emis-sion tomography, PET, and functional magneticresonance imaging, fMRI) have shown thathuman MTþ lies within the ascending limb ofthe inferior temporal sulcus (Huk, Dougherty, &Heeger, 2002;Watson et al., 1993), at the temporaloccipital junction. Similar to striate and early extra-striate cortical regions (Slotnick & Moo, 2003;Slotnick, Moo, Krauss, & Hart, 2002b), MTþhas a retinotopic organization where perceptionof motion in the left visual field is preferentiallyassociated with activity in rightMTþ , and percep-tion of motion in the right visual field is preferen-tially associated with activity in left MTþ (Huket al., 2002; Watson et al., 1993). It has also beenshown that attention to motion increases activityin putative human motion processing regionMTþ (Corbetta, Miezin, Dobmeyer, Shulman, &Petersen, 1990; Liu, Slotnick, Serences, & Yantis,2003; O’Craven, Rosen, Kwong, Treisman, &Savoy, 1997). Furthermore, similar to the contral-ateral attention effects observed in striate andearly extrastriate cortical regions (Corbetta et al.,1990; Liu et al., 2003;O’Craven et al., 1997), atten-tion to motion in the left hemifield preferentiallyincreases activity in right MTþ , and attention tomotion in the right hemifield preferentiallyincreases activity in left MTþ (see, for example,Slotnick & Yantis, 2005).

The results of these neuroimaging studies canbe taken to suggest that human MTþ is involvedin motion perception and attention to motion.However, it is also possible that activity withinthis region is merely epiphenomenal—that is,this region might not be required for motion per-ception (which if true would undermine thisregion’s role in feature-specific processing).A number of lesion studies have attempted toaddress this possibility by correlating sites ofbrain lesions with deficits in motion perception.Specifically, some patients with unilateral pos-terior cerebral lesions have been shown to beimpaired in motion perception in the contralateralvisual field (Barton, Sharpe, & Raymond, 1995;

Braun, Petersen, Schonle, & Fahle, 1998;Greenlee & Smith, 1997; Plant, Laxer, Barbaro,Schiffman, & Nakayama, 1993; Vaina, Cowey,Eskew, LeMay, & Kemper, 2001). Nonetheless,none of these patients had lesions that could bedefinitively localized to MTþ . Indeed, theselesions extended more posteriorly into earliervisual areas (as indicated by contralateral scoto-mas), extended into white matter, included parie-tal regions, and included regions that were notobservable via computed tomography (CT) orMRI. Thus, the contralateral motion perceptionimpairments in these lesions studies mighthave been due to degraded visual processing(caused by lesions to earlier visual regions), discon-nection from another—critical—motion proces-sing region (caused by a white matter lesion), orcontralateral neglect (caused by a parietal cortexlesion). Motion percepts have been reported fol-lowing electrical stimulation to putative MTþ(Lee, Hong, Seo, Tae, & Hong, 2000), andmotion detection impairments have been reportedfollowing transcranial magnetic stimulation(TMS) of putative MTþ (Hotson & Anand,1999; Silvanto, Lavie, & Walsh, 2005; thesestudies did not localize MTþ but rather stimu-lated in the approximate location of this region).In a recent fMRI-guided TMS study by Sack,Kohler, Linden, Goebel, and Muckli (2006),stimulation of MTþ (localized using fMRI) dis-rupted motion perception. To our knowledge,this is the only direct evidence that MTþ maybe necessary for motion perception.

One of our epilepsy patients presented withunusual motion perception phenomena in theright visual field during seizures that was coupledwith both an abnormal electroencephalogram(EEG) over left occipital-temporal scalp (electro-des O1 and T5) and abnormal magnetic resonancespectroscopy (MRS) in the underlying posteriorcortical region. While abnormal MRS is thoughtto reflect altered cortical metabolism, no correlatedanatomical abnormality could be detected withhigh-resolution structural MRI (see Method).Based on this evidence, we hypothesized that hehad a functional lesion (an electro-metabolic dis-turbance without a structural correlate seen on

678 COGNITIVE NEUROPSYCHOLOGY, 2008, 25 (5)

MOO, EMERTON, SLOTNICK

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MRI) in left MTþ . To circumvent the lack oflocalization in lesion studies described above, weconducted a meta-analysis of previous humanmotion processing fMRI studies to independentlyidentify the anatomic location of right and lefthemisphere MTþ (i.e., the regions of interest,ROIs; see Method). The aims of the currentstudy were to: (a) determine whether the patientwas indeed impaired at contralesional motion pro-cessing tasks while being spared at ipsilesionalmotion processing tasks (as our hypothesis wouldpredict); and (b) use event-related fMRI to deter-mine whether such an impairment, should it exist,could be directly linked to decreased motion-related activity in left MTþ (with normalmotion-related activity in right MTþ ) as com-pared to control participants.

Method

ParticipantsThe studies were approved by the InstitutionalReview Boards of Massachusetts GeneralHospital, Harvard University, and Johns HopkinsUniversity and were performed in accordancewith the Declaration of Helsinki.

The patient was a 19-year-old male, evaluatedby the Massachusetts General Hospital EpilepsyService for medically intractable seizures. Prior tomany of his seizures, the patient would complainthat something was “wrong” with his vision, andhe reported, for example, that when talking tohis mother at seizure onset he would see a seriesof her face repeated lateral to her actual face.Visual field testing was unremarkable (indicatingintact striate and early extrastriate cortex function).Neuropsychological testing revealed his IQ to bein the low-average range. He completed highschool requiring minimal special education ser-vices in mathematics only. At the time of testing,he was not driving, was not employed, and livedwith his parents. He denied a history ofdepression, anxiety, or other psychiatric illness.

His EEG demonstrated frequent interictalsharp waves maximal over left occipital-temporalscalp (electrodes O1 and T5; see Figures 1A, 1B).Scalp EEG recordings during his complex partial

seizures demonstrated a similar localization to hisictal onset consisting of high-amplitude rhythmicdischarges in the delta range with maximum ampli-tude at T3/T5/O1 and with particularly sharprhythmic waveforms present primarily at O1throughout the seizure. MRS demonstrated alactate peak in the left temporo-parieto-occipitalregion not seen in the homologous region on theright (Figure 1F). The left hemisphere voxeldemonstrating the lactate peak included thecentre coordinates of left MTþ as defined by theliterature meta-analysis (discussed below). High-resolution anatomic multiplanar rapidly acquiredgradient echo (MP-RAGE, detailed below) andclinical structural MRI scans demonstratedfluid attenuation inversion recovery (FLAIR)/T2hyperintensity and slight volume loss of the lefthippocampus suggestive of mesial temporal scler-osis but no temporo-parieto-occipital abnormal-ities (Figures 1C, 1D, 1E). After informedconsent was obtained, he completed the full-fieldmotion detection task and hemifield motion atten-tion task (behavioural and fMRI protocol) inaddition to the picture identification task (beha-vioural protocol) described below.

The behavioural and fMRI control participantdata for the full-field motion detection task andhemifield motion attention task were taken froma previously published study conducted at JohnsHopkins University; therefore, details are limitedto those relevant to the present investigation(for full details, see Slotnick & Yantis, 2005).Specifically, there were 10 control participants(5 females), all of whom gave informed consent,ranging in age from 21–27 years with normal orcorrected-to-normal vision.

For the picture identification task, behaviouraldata from 10 additional control participants (6females) were acquired at Harvard University,after informed consent was obtained. Thesecontrol participants ranged in age from 18–27years andhadnormal or corrected-to-normal vision.

Behavioural tasks and analysisFor the full-field motion detection task, randomlyarrayed dots (0.058 in diameter) moved toward thecentral fixation point during 14-s motion periods,

COGNITIVE NEUROPSYCHOLOGY, 2008, 25 (5) 679

MTþ LESION IMPAIRS CONTRALATERAL PROCESSING

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which alternated with 14-s stationary periodswhere the dots were “frozen” (Figure 2A). Dotdensity was 1.6 dots/degree2, and dot velocity

was 58/s (where a rectangular visual display forthe control participants was 13.68 � 18.18, andfor the patient it was 24.68 � 32.88). Each

Figure 1. (A). Patient interictal electroencephalogram (EEG) and electrocardiogram (EKG) with amplitude/time scale at centre (vertical

grey lines delineate 1-s intervals). Abnormal activity consisting of sharp waves is evident at electrodes O1 and T5. (B). Scalp model

illustrating a subset of EEG electrode locations (posterior–superior view). (C). Patient high-resolution anatomic multiplanar rapidly

acquired gradient echo (MP-RAGE) axial slice selected to include left and right hemisphere MTþ (left hemisphere toward the left).

(D). Corresponding clinical fluid attenuation inversion recovery (FLAIR) image. (E). Corresponding clinical T2-weighted image. (F)

T2-weighted image with the left hemisphere ROI in which a lactate peak was observed, demarcated by the boxed X.



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control participant completed six or eight motionand stationary periods, and the patient completedsix cycles of each. It is important to note that onthis and subsequent tasks, the patient protocolwas shortened and simplified due to time con-straints and a reduced degree of ability, relativeto control participants. At pseudorandom timepoints during motion periods (i.e., twice permotion period), all of the dots briefly slowed; par-ticipants were trained to press a response buttonwhen this occurred. For the full-field motiondetection behavioural analysis, the hit rate,p(button response)/(slowdown), was computedacross control participants and was compared tothe hit rate of the patient using a one-tailedt test (based on the assumption that the patientshould be impaired, if anything, on the motiondetection task). For this comparison and the sub-sequent behavioural comparisons, p , .05 wasconsidered statistically significant.

For the hemifield motion attention task, movingdots (0.058 in diameter) were bounded by squares inthe left and right hemifields that were rotated 308 ofpolar angle from the horizontal meridian(Figure 2B). Each square was 48 along each edgewith the nearest corner 28 from fixation. Dotdensity was 20.0 dots/degree2 (i.e., 320 dots/square), dot velocity was 58/s, and dot coherencewas 70% (see Newsome & Pare, 1988). Every 14seconds the words “left” or “right” (presented audi-torily) alternated, and participants had beentrained to shift their attention to the correspondingsquare (while always maintaining central fixation).For control participants, left hemifield dots moveddownward, and right hemifield dots movedupward (to avoid perceptual grouping). Dots onthe attended side of the display would speed up orslow down (for 240–400 ms every 2–12 s; magni-tude and duration were tailored for each participantto yield an accuracy of approximately 80%), andcontrol participants pressed a response button ifthey detected a decrease in velocity (or an increasein velocity, depending on prerun instructions). Theprotocol for the patient was nearly identical, exceptfor two changes to ensure that he could adequatelyperform the task (by making it more similar to thefull-field task): (a) The dots in both hemifields

Figure 2. (A). During the full-field motion detection task, the stimulus

alternated between dots moving toward fixation (for 14 s, as indicated

by arrows that were not present in the actual display) and stationary dots

(for 14 s). Participants were instructed to respond when the moving dots

transiently slowed down. (B). During the hemifield motion attention

task, moving dots were continuously presented in both hemifields.

Participants had been trained to interpret the words “left” or “right”

(which were presented auditorily in alternation every 14 s) as cues to

shift attention to the dots in the corresponding hemifield while

maintaining central fixation (dotted circles indicate the locus of

attention and were not present in the actual display). They were

instructed to respond when the moving dots in the attended hemifield

slowed down (or sped up, depending on prerun instructions). (C).

During the hemifield picture identification task, pictures of animals or

athletes that were stationary or had implied motion were briefly

presented to the right or left of fixation. Participants were instructed

to respond whether the object of each picture was stationary or

reflected implied motion while maintaining central fixation.



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moved toward fixation (rather than upward ordownward); and (b) he was only presented withand had only been trained to respond to decreasesin dot velocity in the attended hemifield (ratherthan decreases or increases in velocity). All of thecontrol participants completed two runs in thescanner (which were used for both behavioural andimaging analysis) while the patient completed onerun outside of the scanner followed by two runs inthe scanner (all three runswere included in the beha-vioural analysis to maximize power). For the hemi-field motion attention behavioural analysis, the hitrate was computed for the left and right hemifieldsacross control participants (which were comparedto one another using a two-tailed t test), and eachof these values were compared to the respective hitrate for the left and right hemifields of the patientusing a one-tailed t test (again, with the assumptionthat the patient should be impaired). In addition, todetermine whether the patient showed specificimpairment in the contralesional hemifield (usingthe ipsilesional hemifield as a within-patientcontrol), hits and misses associated with the leftand right hemifields were entered into a one-tailedFisher exact test.

In the hemifield picture identification task,black-and-white pictures of athletes or animalsthat were stationary or had implied motion (i.e., asnapshot of an athlete or animal in motion) werepresented to the right or left of fixation(Figure 2C; see Kourtzi & Kanwisher, 2000).Due to time limitations, the patient and a new setof 10 control participants (6 female) completedjust the behavioural portion of this task. Pictureswere approximately 28 in width and height andwere centred on the horizontal meridian with thenearest edge 28 from fixation. For each of tworuns, 80 pictures (20 of each type, randomly inter-mixed) were briefly presented (250-ms duration)every 4 seconds. While maintaining central fix-ation, control participants and the patient hadbeen trained to press one button if the picture wasstationary and another button if the picture hadimplied motion. The stimuli for the second runwere identical to those for the first run in allrespects, except that they had been flipped horizon-tally about fixation. In this way, the stimuli were

counterbalanced over hemifield of presentation,the factor of interest. For the hemifield pictureidentification analysis, the patient did not showany differential responses to stationary pictures inthe left and right hemifields (Fisher exact test,p . .20). As such, the hit rate for implied motionpictures, p(“motion” button)/(implied motionpicture), was used to conduct all the same compari-sons as for the hemifield motion attention task.

Imaging acquisition and analysisControl participants for the full-field motion detec-tion and hemifield motion attention tasks werescanned using a Phillips ACS-NT 1.5 Tesla MRIscanner, where anatomic images were acquiredusing a T1-weighted multiplanar rapidly acquiredgradient echo (MP-RAGE) sequence (time to rep-etition, TR¼ 8.1 ms; echo time, TE ¼ 3.7 ms; flipangle ¼ 88; isotropic resolution 1 mm), and func-tional images were acquired using a T2�-weightedecho planar imaging sequence (TR ¼ 2 s;TE ¼ 40 ms; flip angle ¼ 908; 26 slices; no gap; iso-tropic resolution 4.5 mm). The patient was scannedusing aSiemensAllegra 3TeslaMRI scanner,whereanatomic images were also acquired using anMP-RAGE sequence (TR ¼ 30 ms; TE ¼ 3.3 ms;flip angle ¼ 408; resolution 1 � 1 � 1.33 mm),and functional images were acquired using a T2�-weighted echo planar imaging sequence (TR ¼ 2 s;TE ¼ 30 ms; flip angle ¼ 908; 35 slices; no gap;isotropic resolution 4 mm). All data analysis wasconducted using BrainVoyager (Brain Innovation,Maastricht, The Netherlands). Functional datapreprocessing included slice time correction,motion correction, and high-pass temporal filteringto remove components below 3 cycles per runlength (no spatial filtering was conducted).

A general linear model approach was used forthe full-field motion detection imaging analysis.Specifically, for each participant, the square-wavedefining the periods of moving dots and thesquare-wave defining the periods of stationarydots were each convolved with a canonical hemo-dynamic response function to produce a model ofeach event type (moving dots and stationarydots). A general linear model was used to fitthese two models to the activation time course of



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each voxel in the functional volume to produce theassociated model amplitudes (i.e., beta-weights).Then, the voxels/brain regions associated withmotion perception (and attention to motion)were identified by conducting a statistical contrastbetween the beta-weight for the moving dots andthe beta-weight for the stationary dots. For indi-vidual participant analysis, these “active” regionswere then painted on a surface reconstruction ofthe brain, produced by segmenting each hemi-sphere at the grey/white matter junction.Control group activity was also identified using arandom effect analysis. For all comparisons, anindividual voxel threshold of p , .05 was used(to avoid Type II error), and a cortical surfacecluster extent threshold of 135 mm2 was enforcedto correct for multiple comparisons to p , .01.

To assess the degree to which motion perception(as compared to stationary dot perception) evokedactivity in human motion processing complexMTþ , a meta-analysis of eight studies wasconducted to independently identify the lefthemisphere MTþ and right hemisphere MTþTalairach coordinates (Beauchamp, Lee, Haxby, &Martin, 2002; Kourtzi, Bulthoff, Erb, & Grodd,2002; Liu et al., 2003; Rees, Friston, & Koch,2000; Sunaert, Van Hecke, Marchal, & Orban,1999; Watson et al., 1993). Left hemisphereMTþ had a range of x ¼ 242 to 248,y ¼ 264 to 270, and z ¼ 22 to 2, with a meanof x ¼ 245, y ¼ 267, and z ¼ 1, while righthemisphere MTþ had a range of x ¼ 40 to 50,y ¼ 260 to 273, and z ¼ 21 to 6, with a meanof x ¼ 45, y ¼ 266, and z ¼ 1. The ranges of leftand right hemisphere MTþ coordinates from themeta-analysis were used to define ROIs. It shouldbe noted that this method is particularly powerfulgiven that the ROIs were defined independently,from the literature, and thus can be considered anobjective way to localize MTþ (which was necess-ary given that the patient was hypothesized to have afunctional MTþ lesion).

The hemifield motion attention imaging analy-sis used an ROI event-related time course analysisapproach (Slotnick, 2005). That is, for each partici-pant, the left and right hemisphere ROIs weredefined as the mean Talairach coordinates from

the MTþ meta-analysis (described above). Theactivity time course (from 2 2 to 20 s followingevent onset) associated with attention to movingdots in the left hemifield (attend left) was extractedfrom each ROI, as was the attend right time course.Time courses were baseline corrected (to a mean ofzero) from 2 to 0 s preceding stimulus onset andwere corrected for linear drift. Attention effectswere assessed between 6 and 14 s following stimulusonset, as this was the expected period of sustainedattention-related activity (due to the time lag ofthe haemodynamic response). Based on theknown contralateral sensory effects of attention(Brefczynski & DeYoe, 1999; Martinez et al.,2001; Slotnick, Hopfinger, Klein, & Sutter,2002a; Slotnick, Schwarzbach, & Yantis, 2003;Tootell et al., 1998), the magnitude of attentioneffects were computed by taking the differencebetween contralateral and ipsilateral mean activitymagnitudes (which is discussed in more detailbelow). First, to confirm that control participantshad attention effects in the left and right hemi-sphere MTþ , a one-tailed t test was used to deter-mine whether these values were significantlygreater than zero (while a two-tailed t test wasused to directly compare them). Then, the patient’sleft and right MTþ attention effect was comparedto the respective control participants’ attentioneffects using a one-tailed t test (with the assump-tion that the patient would have a deficit).Additionally, to further assess whether the patienthad a specific impairment in the purportedlylesioned (left) MTþ , his left hemisphere attentioneffect was directly compared to his right hemi-sphere attention effect (using between-trial varia-bility to estimate variance).

Poststudy confirmation of epileptogenic regionIn the course of the patient’s ongoing epilepsy-related clinical care, he elected to undergo invasiveepilepsy monitoring aimed at more precisely loca-lizing his seizure onsets to determine his candidacyfor a surgical intervention in an effort to control hismedically intractable epilepsy. More specifically,given the patient’s lack of conclusive data basedon scalp EEG recordings regarding the preciselocalization of his seizure onsets, in an effort to



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potentially localize a single seizure focus that couldbe surgically resected to reduce seizure frequency,he underwent a left temporo-parietal craniotomyunder general anaesthesia for placement of a 48-contact subdural electrode grid (1 � 1 cm inter-electrode distance) on the cortical surface of theleft posterior temporo-parieto-occipital region.

Intraoperatively, passive electrocorticographywas performed and revealed spontaneous epilepti-form activity consisting of spikes, polyspikes, andsharp waves (electrographic signatures indicatinglikely seizure onset) in runs of up to 20 s arisingfrom the posterior aspect of the inferior temporalgyrus (i.e., the known anatomic locus of humanmotion processing region MTþ ).

Results

BehaviouralFigure 3 illustrates the behavioural results. For full-field motion detection (Figure 3A), the patient wasvery accurate (hit rate ¼ .92) and performedsimilarly to controls (hit rate ¼ .94 + .03;t ¼ 1.07, ns). For hemifield motion attention(Figure 3B), controls were able to detect changesin dot speed in the left visual field (LVF; hitrate ¼ .80 + .04) and the right visual field(RVF; .77 + .06) to a similar degree (t , 1).The patient, in this task, showed impaired per-formance versus controls in both the LVF (hitrate ¼ .54; t ¼ 7.00, p , .001) and the RVF(hit rate ¼ .33; t ¼ 7.29, p , .001). Critically,RVF (contralesional) performance was moreimpaired than that in the LVF (Fisher exact test,p , .05). For hemifield picture identification,specifically for implied motion pictures, the samepattern emerged (Figure 3C; as mentioned pre-viously, there was no differential response tostationary pictures across hemifields, p . .20).Controls identified implied motion pictures in theLVF (hit rate ¼ .76 + .04) and in the RVF(.76 + .04) to a similar degree (t , 1), while thepatient was impaired in both the LVF (hitrate ¼ .63; t ¼ 3.89, p , .01) and the RVF (hitrate ¼ .41; t ¼ 9.55, p , .001). Of most import-ance, contralesional implied motion identificationperformance in the RVF was more impaired than

Figure 3. (A). Hit rate associated with full-field motion detection for

control participants (controls) and the patient. For controls,

mean + one standard error reported. (B). Left visual field (LVF)

and right visual field (RVF) hit rates associated with hemifield

motion attention for controls and the patient. (C). LVF and RVF

hit rates associated with hemifield picture identification for controls

and the patient (restricted to pictures with implied motion).



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that in the LVF (Fisher exact test, p , .05). Thiswas further supported by a significant item type(stationary, implied motion) by hemifield inter-action (p , .001).

Functional neuroimagingFigures 4 and 5 illustrate the fMRI results.Figure 4 shows motion-related functional activityas defined by the full-field motion contrastbetween moving dots and stationary dots. For allcontrols (Figure 4A), activity extended into theMTþ ROIs of both hemispheres (defined froma meta-analysis of the literature; see Method)shown by the blue ellipses. For the patient(Figure 4B), activity extended into the rightMTþ ROI but did not extend into the leftMTþ ROI (which was 11 mm from the nearestactivity). Figure 4C illustrates an enlarged viewof the cortical surface surrounding the patient’sleft MTþ ROI, with the control group activityshown in blue (this activity extended into theMTþ ROI within the ascending limb ofthe inferior temporal sulcus) and the patient’smotion related activity shown in red (with overlap-ping activity in purple). It is notable that patient’sfull-field motion-related activity was not found oneither the posterior or anterior banks of the leftinferior temporal sulcus, as these anatomiclocations have been associated with humanmotion processing regions MT andMST, respect-ively (Beauchamp, Yasar, Kishan, & Ro, 2007;Huk et al., 2002), suggesting that the patient’sfunctional lesion includes human motion proces-sing region MT at a minimum. Other regions ofmotion-related activity (e.g., parietal and frontalcortex) were also observed (Figure 4A, 4B) andcan be attributed in part to sustained attention(see Slotnick & Yantis, 2005) during periods ofmoving dots versus stationary dots; however,these regions are not considered further as theyare not relevant to the hypothesis under investi-gation. Consistent with the contrast results,activity extracted from the patient’s right MTþROI showed a robust motion-related increasein activity while activity in the left MTþROI showed little motion-related modulation(Figure 4D; this differential effect in the right

MTþ was significantly greater than that in theleft MTþ , t ¼ 2.99, p , .01). These results areconsistent with a functional lesion in the patient’sleft MTþ .

Figure 5 shows the attention-related activityassociated with the hemifield motion task. Forcontrols (Figure 5A), replicating previouslyobserved contralateral visual area attentioneffects, there were increases in MTþ activityduring attention to the contralateral hemifield(i.e., increases in left MTþ with attention to theRVF and vice versa for the right MTþ ).Although this contralateral attention effect wasalso observed in the patient’s right MTþ , therewas no such effect in the patient’s left MTþ(Figure 5B). For controls, a significantly positiveattention effect was observed in the left MTþ(0.19 + 0.07; t ¼ 2.73, p , .05) and the rightMTþ (0.14 + 0.06; t ¼ 2.37, p , .05), andthese effects were similar in magnitude (t , 1).The attention effect in the patient’s left MTþwas negative and significantly less than that ofcontrols (2 0.02; t ¼ 3.01, p , .01), providingfurther evidence for a functional lesion withinthis region. Of additional interest, the attentioneffect in the patient’s right MTþ was significantlygreater than that of controls (0.51; post hoct ¼ 6.30, p , .001), which is discussed immedi-ately below. The attention effects in the patient’sleft and right MTþ were also significantly differ-ent (t ¼ 2.2, p , .05).

Discussion

Behaviourally, this patient with electrophysiologi-cal and metabolic evidence of a unilateral func-tional temporal-occipital lesion was not impairedon the full-field motion detection task, but his per-formance in both hemifields was impaired on thehemifield motion attention task and the hemifieldpicture identification task. The patient’s unim-paired performance on the full-field motiondetection task could have been due to a ceilingeffect, where this task was too easy to reveal amotion-processing deficit. In support of this possi-bility, controls found the full-field motion detec-tion task less difficult (i.e., it was associated with



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Figure 4. (A). Cortical surface reconstruction of 10 controls (lateral views, left hemisphere toward the left, superior toward the top; light and

dark grey represent gyri and sulci, respectively) with motion-related activity defined by the moving dots . stationary dots contrast in the full-

field motion detection task (red to yellow indicates increase in significance). The left and right MTþ regions of interest (ROIs), demarcated by

blue ellipses, were defined via a meta-analysis of the literature. Motion-related activity for every control participant extended into both left

and right MTþ ROIs. (B). Patient cortical surface reconstruction with motion-related activity and MTþ ROIs. Although motion-related

activity extended into the right MTþ ROI, it was absent from the left MTþ ROI. (C). Enlarged view of patient’s left hemisphere proximal

to the left MTþ ROI (demarcated by the blue ellipse). The patient’s motion-related activity is shown in red, the control participant group

activity is shown in blue, and overlapping activity is shown in purple. (D). Event-related time courses extracted from left and right MTþ

ROIs of the patient (at centre coordinates defined by the literature meta-analysis; see key at centre). The solid vertical white line indicates

event onset while the dotted vertical line indicates event offset.



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higher accuracy) than both the hemifield motionattention task (t ¼ 3.14, p , .01) and the hemi-field picture identification task (t ¼ 4.20,p , .001; post hoc one-tailed t tests). As such,the patient may have had a general motion-processing deficit within both hemifields, whichwas only revealed under sufficiently difficult taskconditions. That is, the patient may have simplyfound the tasks generally more difficult than didthe controls (given that it was not possible tomatch such factors as seizure history, IQ, andlevel of education). It is also possible that thedecrement in left visual field performance may

have been due, in full or in part, to the functionallesion in left MTþ , as MTþ has also been shownto process motion to some degree in the ipsilateralhemifield (Dukelow et al., 2001; Huk et al., 2002;Tootell et al., 1995). Although a lesion in thepatient’s right MTþ could also explain the beha-vioural results, our imaging evidence showednormal motion processing in this region(Figure 5). The critical finding was that therewas significantly worse performance in the rightvisual field than in the left visual field. If taskdifficulty was the only reason for the patient’sperformance impairment, a similar accuracy decre-ment would be expected in both the right and lefthemifields. Thus the significant differential hemi-field accuracy is consistent with a functional lesionin left MTþ .

The present results complement previous find-ings of contralateral motion-processing deficits inpatients with unilateral posterior cortical lesionsdue to stroke, tumour, or surgical resection(Barton et al., 1995; Braun et al., 1998; Greenlee& Smith, 1997; Plant et al., 1993; Vaina et al.,2001). However, as mentioned previously, it isinherently difficult to define the extent of patientstructural lesions and their relationship to normalcortical anatomy. Because we used an independentmeta-analysis to identify the loci of left and rightMTþ , and our patient had no evidence of grossstructural lesion in the area, our results are, toour knowledge, the most precise example of a uni-lateral MTþ lesion evoking contralateral motionprocessing deficits to date. Additionally, the post-study direct electrocorticography demonstratedspontaneous epileptogenic activity in a relativelysmall circumscribed region within the temporal-occipital cortex. As with the coupling of lesion-deficit studies and those using direct neuronalstimulation to alter motion percepts in monkeys(Newsome & Pare, 1988; Salzman, Britten, &Newsome, 1990), our convergent pattern of beha-vioural results and imaging findings provide com-pelling evidence that human MTþ is a necessarycortical region for motion processing.

Our results also have an importantmethodologi-cal implication with regard to the degree to whichfMRI activity accurately reflects neural processing.

Figure 5. (A) Hemifield motion attention task event-related

activity time courses extracted from left and right MTþ ROIs of

controls (at centre coordinates defined by the literature meta-

analysis). Attention to the right visual field (RVF) evoked

increased activity in left the MTþ , and attention to the left

visual field (LVF) evoked decreased activity in the left MTþ ,

while attention to the LVF evoked increased activity in the right

MTþ , and attention to the RVF evoked decreased activity in the

right MTþ (see key). (B) MTþ ROI event-related time courses

for patient. Although the same pattern of contralateral attention

effects can be observed in the right MTþ , there were no

attention effects in the left MTþ .



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fMRI activity is widely assumed to reflect neuralactivity associated with a given task, and indeedfMRI activity has been shown to correlate withneural activity in the same region (Logothetis,Pauls, Augath, Trinath, & Oeltermann, 2001).However, the degree to which such activity isnecessary for a given task as opposed to epipheno-menal is frequently irresolvable. The only way todetermine whether a neural region is in fact necess-ary for a given process is to investigate the conse-quences of a temporary lesion (e.g., via TMS) oran existing lesion in that area (e.g., due to strokeor other type of lesion, as in the present case). Assuch, the present functional lesion results, whichcomplement the recent TMS findings of Sacket al. (2006), can be considered a validation of pre-vious studies that have assumed that fMRI activityin human MTþ reflects motion processing.

Manuscript received 5 September 2007

Revised manuscript received 13 May 2008

Revised manuscript accepted 13 June 2008

First published online 23 July 2008

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Functional MT + lesion impairs contralateral motion processing