Neuropsychologia, Vol. 22, No. 2, pp 187-196. 1984. Prmted in Great Bntam

0028-3932/84 $3.00+0.00 (‘ 1984 Pergamon Press Ltd.

ALTERATIONS IN VISUALLY RELATED EYE MOVEMENTS FOLLOWING LEFT PULVINAR DAMAGE IN MAN

MARILEE P. OGREN*

Department of Psychology, Massachusetts Institute of Technology, Cambridge, MA 02139, U.S.A

CATHERINE A. MATEER and ALLEN R. WYLER

Department of Neurological Surgery, University of Washington School of Medicine, Seattle, WA 98195, U.S.A.

(Accepted 11 October 1983)

Abstract-This case study presents evidence for two subtle types of eye movement abnormalities following surgical resection of the left posterior pulvinar in man. First, visual fixations during vertical pattern matching are on average both increased in number and prolonged in duration compared to controls, although normal fixation durations also occur. Second, unilateral deficiencies during search and scanning performance are associated with eye movements directed into the hemifield contralateral to the lesion. Although direct damage to parietal cortex and indirect damage to other visually related structures cannot be ruled out as other explanations for these deficits, these findings are consistent with recent electrophysiological and behavioral studies of the pulvinar in both human and non-human primates, and suggest a fruitful area for further investigation of pulvinar function.

INTRODUCTION

COMPARED with other mammals, the pulvinar nucleus in primates is large relative to the other thalamic nuclei, and dominates the posterior one-third of the thalamus. It is generally thought that the elaboration of the primate pulvinar is a recent phylogenetic development, related to the expansion of neocortex. The function of pulvinar in mammals in general, and the reasons for its expansion in primates, however, are still unknown. Some investigators report no observable behavioral deficits following pulvinar lesions in monkey [9, 19,343 and man [lo, 291, although there is ample neuroanatomical [2, 3, 4, 5-7, 21-23, 321 and electrophysiological [l, 13,27,30] evidence for pulvinar involvement in visual function, and some behavioral evidence for a role for the pulvinar in visual performance [S, 33, 351. Of particular interest for the present study are behavioral and electrophysiological findings in monkeys [27, 301 and humans [31] that point to the importance of the pulvinar in visual fixation and saccadic eye movements. We present additional evidence in this report of a single case study which suggests that pulvinar damage in the human results in disruption of eye movement behavior associated with visual performance.

CASE HISTORY A 23-yr-old male patient, without significant medical history, sustained hemorrhage of an arteriovenous

malformation (AVM) in the posterior portion of the pulvinar nucleus of the left thalamus. A trans- cortical- transventricular approach via a left parietal craniotomy was used to resect the AVM. A CT scan taken

*To whom reprint requests should be addressed.

187

8 months post onset (Fig. 1) revealed a smaller left thalamus with localved tissue loss in the rrglon of the pulvinar. There was also an associated enlargement of the left lateral ventricle and local dilatation of the third ventt~cle.

In the early pw(-operative period, the patient demonstrated a mIlti aphasia. confusion. right-sided beahness and ataxic gait. All symptoms resolved and at the time of cisual testing. 21 weeks after surgerv, he was orlented. his gait was essentially normal and his speech was without aphasic errors. Res:dual language de&its included a mild anomia and difficulty wth short-term verbal memory. The visual deficltj \\ere first suspected during the language testing when he demonstrated a marked difficulty m rending in rhe absence of characterl<tically aphasic errors.

On neuro-ophthalmological testing, rhe patient v+as Judged to have subtle difficulty with \azcadlc !nltiallon. variability in saccadic pursuit and a subtle disturbance ofsustained fixallon. Convergence wxs I + 4$ In contrast to these eye movement disturbances, his pupil% were normal, extraocular muwleh iveere inkact, awit) was unchanged and rhere was no evidence for a gross visual field defect to confrontation. He ~\a> able to correctly identify J geome(rtc shape embedded in a random dot aterogram [ 151. indicating the presence of steropsls. ‘Thele ~‘a\ no suggestion of gross visual neglect on a simple geometric figure copy, cancellarion tasks or line hlrection. He d~cl demonstrate a tendency lo \tar-e fixedly for extended periods of time even whtle spcaklng or being spoken 10

METHODS fhe patlent and Iwo non-hospitalized male5 (control bubjccts 1 and 2i marched to rhe pa~lent fat .~gc: and

educational history were adminIstered all tests. Nelthcr control had any hi\torq of neurological or 1 isu‘il Impail ment, and none of the three uore corl.ecilvc lcn.,es.

(A) Pafrarn wm/dting. Visual pattern dlscrinunatlon \\a\ meawted for three ample type\ of figure\: of lented Ilne\, line drawmgs offamdiar figures, and photographs of male faces [I I’]_ These figures \+crc prewned h) slide\ rhal u ere rear projected onto a screen approximately 45 cm from rhe huhject. The head was not rigidly held Indi\ldual discriminanda subtended approximately IO’ of wsuai angle In each trial a group of four discriminanda (line\, Ilnc drawings or photographs) were organized vertically. The ta& was to indicate cerballq M hich one ofthe lov,el th:-cc (labeled A, B and C) was an exact march of the sample at the top. Ten trials uere gown for each of these t!;w <),f figures. Accuracy and latency were recorded for each II-I~~. The whjects’Face.s welt \ldcolaped during each 1r1a1 fol analyGs of eye movemenl~ as descrlhecl in B

(B) EJL, mownw~~ Y tlro.in~~ ,~crrrrrn mlrr(-hiny: /LYU~W~I nw~lw ut~l Jwuriotl Fyc movcnxmt\ \\ ere recorded u\:ng a Qluasar Model No VH5160 video recorder, connected to ‘! camera (R(‘A NC,. 5(‘1005) nith ‘I 25 mm lenr Lhat v.a\ fixed 45 cm from the wb_iect at a 45’ angle from the line of Tight. The lrame format wa: 30 frames per second 4 COIIJ C’VM 131 video monitor MS used to meawre fixation duration dul-ing \Iov. motion playback hy cuunting tllc number offrames that elapsed during each fixation. 1 he to!al number of fixation? that wcurrcd be:tween Ihe imwl ill Ihe tirscrirninanda (observed in cornea1 reflection) and rhe Imtlatlon of the wponue (lip movement) wa\ aiw counted. Movemenir that did not Iresult In stable Iixa~ions for three flames 01 ~noi-c 10. I ‘ICC) M cl e co:~s~liered it\ inter-mediate stage:. of saccades and uere ,101 counted Becauw ihere wrc no signtficanl dtffcrcncc\ aclo, the three matching tasks. measllreb of accurac!, rwponsc latency and eqe movements \cerc ~ollapw! acrcIss iasks.

(C) K<J,‘s /<wg/ed lirm LX]. In this test. I6 horlrontaliy oriented by irregular jagged lines IapproxImately 25 c‘m m length) which iniersect at obhque and rIglit angles v+crc presenwd on a card. l’hc endpoint\ ~,l each hne \\erc numherzd diffcrentlq at their right and left margins. The !,ubjecl’\ tusk \&as to \ ~wally follo,u one line from hcgmnmg to end. E-our trials I-cquircd trackmg from lrft to I lght and fout- from right lo left. Viewing di?tanL,e v a\ nor tixed. The \Itie and number at hhlch to begin were glvrn \crh:~ll) and response tlmcs for co1 I-WI twls v+er-e I-ecordcd 1n wzontls.

Two major findings in this study show evidence for abnormalities foilowing surgical resection of the left posterior pulvinar: (1) rhe number and duration of’ visual fixations increase during pattern discrimination, and (2 I \ iwal hollowing and <earth associated with the contralateral hemifield are impaired. I he fir’rt of these deficits is shown in the patient’s bcha\ior during pattern matchin!; (,4. E3 in Methods). and !he second 111 his performance on

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CONSEQUENCES OF HUMAN PULVINAR DAMAGE 191

Rey’s tangled lines and the visual search task (C, Din Methods). Both of these deficits appear to be associated with alterations in eye movements.

Pattern matching and eye movement analysis

In each of the three pattern matching tasks, the control subjects performed the visual discriminations rapidly and without error. The mean response latencies across tasks was 1.9 set for both control subjects. In contrast, the patient made errors or exhibited self-corrections on eight of the 36 matching tasks; and showed a striking increase in response latency (5.9 set) for correct matching trials which was three times longer than that of the controls (Table 1).

This increase in the patient’s response latency during pattern matching is associated with the large number and long duration of eye fixations required before solving the task. He differed markedly from controls in both of these measures, as his fixations were more than three times as numerous and were on average twice as long as controls (Table 1). As shown in Fig. 2, approximately half of the fixation durations for control subjects fell within the 0.1-0.3 set range, and none exceeded 0.9 sec. In contrast, 40% of the patient’s fixations were 0.9 set or longer, and could be as long as 2.3 sec.

It was apparent from the video tapes of their performance on this task that both control subjects used the same strategy. Before the slide was illuminated, they anticipated the position of the comparison item at the top of the slide, and after it appeared they fixated briefly and only once on each of the three discriminanda before responding: hence an average ofthree fixations per trial of approximately 0.3 set each. Subjectively they found the task very simple. The patient’s strategy was different. Although he anticipated the position of the first item at the top of the slide before it was illuminated like the controls, he subsequently made extended and repetitive fixations on each of the items before responding, resulting in his longer average response time.

Rey’s tangled lines

The patient’s behavior on this task differed from controls only for lines that were followed from left to right: into the field contralateral to the lesion (Table 2). Each of the control subjects followed each of four lines rapidly and correctly from left to right. and as well on all but one trial in one control subject, from right to left. In contrast, while the patient followed all four lines from right to left without difficulty, he could not visually follow any line from left to right. Curiously, he was able to track from left to right if he was allowed to trace the line with his finger.

Table 1. Vertical pattern matching

Ke5ponse latency

(set) Fixation number

Fixation duration

(set) -

Control 1 ?I=36 I .9 (0.79) 3.2 (1.5) 0.32 (0.1’) Control 2 n=36 1.9 (0.581 2.9 (1.1) 0.37 (0.18) Patient n=ZX 5.9 (3.06) 10.0 (4.2) 0.70 (0.45)

The mean response latencies, mean number and durations of fixations per trial and standard deviations (parentheses) for correct trials of the \;ertlcal pattern matching task. Scores are collapsed over three dlfferent types of dlscriminanda.

192

FIXATION DURATION

ISea

F I(;. 2. Percent and range of visual tixatlon durations are shown for the patient (black bars) and two control subjects (shaded and hatched bars). The percent number of fixations made withln each of the arbitrary fixation duration ranges overlap for the patient and controls at short durations. but 40”,, of

the patient’s fixations were 0.9 L;ec in duration or longer.

Table 7. Rey’b tangled 1Int.b. Mean Irespon\e latencles

Control I Control 7 Patient

Right to left Left to right

9.3 set (2.X7) II=-4 7.4 set (1.X9) ?I = 4 7.2 set (1.04) II = 3 6.9 set (0.67) ?I = 4

10.5 set (2.38) iI = 4 * II = 0

The mean and standard de\lation (parentheses) for response laterues for each correct trial on Rey‘s tangled lines. Scores for lines tracked from right to left are shown in the left column. and !hose for left to right are shown in the right column.

*Note that none of the patient‘s attempts to scan tn the direction contralateral to the lesion were successful, in contrast to hts near normal performance for Ilnes scanned toward the lpsilateral side.

Visual search

The two control subjects performed this task without error on each of ten trials in under 7 set (Table 3). The patient on the other hand located only five of the ten matching drawings within the 60 set allowed per trial. Moreover, each of the five that he located were on the left side of the array. No matches were made with items on the right side of the array. His mean search time on correct trials was more than twice that of controls and showed greater variability, which is consistent with his performance on vertical pattern matching tasks.

DISCUSSION

This patient demonstrated alterations in his visual behavior following left pulvinar hemorrhage and surgical resection. Compared to normal subjects, his ability to discriminate vertically oriented simple forms and faces was reduced, and during such discriminations his visual fixations were more numerous and more prolonged than controls. He was also impaired on tasks that required visual following and searching behavior into the field contralateral to the lesion. These findings suggest that damage to the pulvinar in this patient disrupted neuronal circuits that are related to the control of eye position during visual

CONSEQUENCES OF HUMAN PULVINAR DAMAGE

Table 3. Visual search

193

Mean response latencies

Control 1 6.3 set (2.07) n=lO (5 left, 5 right) Control 2 6.1 set (4.12) n=lO (5 left, 5 right) Patient 16.8 set (8.81) It= 5 (5 left, 0 right)

The mean and standard deviation (parentheses) for response latencies on correct trials of the visual search task. Note that the patient was unable to locate objects on the right side of the array, i.e. contralateral to his lesion, and his latency to locate objects on the left is protracted.

performance. Before discussing the perceptual or motor nature of these deficits and the relationship to pulvinar organization, we must consider the potential involvement of other brain structures.

The patient’s initial ventricular hemorrhage with attendant hydrocephalus, and the surgical tract through the high left parietal cortex, represent additional areas of neurological involvement beyond the pulvinar. The initial constellation of deficits immediately following surgery, including confusion, right-sided weakness and ataxic gait, reflect a much larger functional lesion at that time, probably associated with hydrocephalus. These symptoms, however, had cleared by the time of visual testing and examinations of CT scans taken 2 weeks post onset (not shown) indicated that the hemorrhage and hydrocephalus had subsided. The patient did show a residual anomia and a deficit in short-term verbal memory. These effects, however, have previously been reported in conjunction with left lateral pulvinar lesions or stimulation [ 16, 251 and thus might be expected from disruption of the pulvinar alone. The area of superior parietal lobe through which the surgical approach was made has been associated with sensory neglect syndromes [17], so that its potential involvement in the present findings cannot be ignored. The approach was made, however, through a small vertical cut made parallel to the descending and ascending fibers, and as such would constitute minimal direct damage to parietal cortex and associated fiber pathways.

Of greater concern to us is secondary damage to frontal, parietal and temporal cortex because in primates these areas constitute major targets for posterior pulvinar efferents, and in turn send reciprocal afferents back to the pulvinar (reviewed in [24]). Thus secondary anterograde and retrograde degenerative changes in cortex resulting from pulvinar damage are unavoidable. Indeed, evidence of decreased cortical function in association with primary thalamic damage in man has been documented with positron emission tomography [18]. Furthermore the superior colliculus and pretectum, which play major roles in oculomotor control, receives fibers from the retina and from the cortex by means of pathways that pass through and around the pulvinar. The superior colliculus also projects to anterior portions of the pulvinar nucleus [3, 261, and although the lesion in this patient was made posteriorly, probably in medial and lateral pulvinar subdivisions, potential involvement of inferior pulvinar and fiber tracks of the tectum cannot be excluded. In addition, there is evidence for direct input from the pretectum to posterior pulvinar [S]. Thus the anterograde and retrograde changes in the cortex and the potential involvement of superior colliculus and pretectal fibers could contribute to alterations in visual behavior following this posterior pulvinar lesion. In these respects, it is inappropriate to speak of a discrete focal lesion in the pulvinar. With this proviso we assume that the behavioral changes shown in this study

primarily reflect substantial direct damage to the posterior portion of the left pulvinar, and secondarily to interruption of the cortico-thalamic and tectal connections.

Alterations in fixation during pattern matching

The findings concerning an increase in fixation duration in our patient are in good agreement with previous reports by UNGERI.EIIER and C‘HRISTENSEN [33, 351 on eye movement alterations in macaque monkeys following pulvinar lesions. These authors have shown a two-fold increase in mean fixation time in their Iesioned monkeys compared to

normals, just as we have shown in the present study. Their monkeys. like this human patient, were also capable of making short fixations as well. UNG~RLEIDER and CHRISTENSEN [33, 351 also report that their lesioned monkeys exhibited “visual capture” as they made fewer than normal saccades during spontaneous scanning and time limited visual discrimination tasks. Similarly. this patient also appeared to stare fixedly for long periods of time. and his fixations during visual discrimination were Indeed prolonged. In addition, he required at least three times the normal number of fixations during the unlimited time in which he was allowed to make a correct discrimination response. For any short period of time, however, his fixations were necessarily fewer because they were longer in duration, and in this respect fit the description of visual capture.

This patient’s degraded accuracy in pattern matching was unexpected because several previous studies report no deficit in visual discrimination following pulvinar lesions in monkey 19, 10, 19, 33-3.51. Only one study of pulvinarectomized monkeys [8] shows a marked impairment in visual discrimination; however, those lesions were primarily anterior in the nucleus and the stimuli were presented tachistoscopically. At present it is unclear what aspect of our paradigm is responsible for this deficit, and further behavioral studies in lesioned monkeys are required in order to specify its nature.

Asymmetries in Lima1 seirrch antl,fbllowir~y

In addition to changes in pattern matching and eye fixation behavior following left pulvinar damage, this patient also demonstrated marked asymmetry on tasks that required him to engage in complex searching or scanning into the hemifield contralateral to his lesion. He did not demonstrate visual neglect on simple figure copying, line bisection, compound word reading or line cancellation, and had no extinction to bilateral simultaneous tactile. auditory or visual stimuli. Furthermore, clinical testing did not show any gross abnormalities in proficiency on the full range of eye movements. As such, the asymmetries in visual search and scanning suggest a form of visual neglect associated with eye movements directed into the field contralateral to the lesion.

Classical forms of unilateral neglect have been associated with damage to the inferior parietal lobe 114, 171, frontal lobe and cingulate cortex [I 1. 361 as well as to subcortical structures including portions of the brainstem, basal ganglia and thalamus [ll, 37,381. This patient may provide another example of a form of unilateral neglect following damage to a subcortical structure. Recent electrophysiological evidence that is consistent with this finding shows that pulvinar neurons in monkey discharge during and after contralaterally directed saccades [30]. In addition, it has been suggested that EEG and Tingle urut activity in the human pulvinar is associated with saccades and attentive fixations [31]. In view of the fact that unilateral neglect is commonly more frequent and persistent following right rather than left hemisphere lesions, it is noteworthy that these authors [3 l] also suggest that units in the right pulvinar fire in association nith saccades into both left and right visual fields, while

CoNStQUtNCES OF l<UMAN PULVINAR UAMAtiF 195

units in the left pulvinar fire in association only with saccades into the contralateral right field. This finding needs substantiation, but nonetheless suggests that with a right-sided pulvinar lesion, the contralateral deficit might be more pronounced.

It should be emphasized that the posterior pulvinar has extensive reciprocal connections with the inferior parietal lobule, temporal and frontal cortex, including the frontal eye fields (see [24]). As such, destruction of the pulvinar may result in loss of integration between it and these cortical areas due to interruption of reciprocal pathways, and potentially to secondary degenerative changes in cortex. Moreover, both the inferior parietal lobule and frontal cortex have been implicated in neglect phenomena and eye movement behavior [ 11, 14, 17,361, so that dysfunction of these areas secondary to the loss of pulvinar connections, or because of direct damage to parietal cortex during surgery, may contribute to the visual neglect and eye fixation abnormalities observed in this patient.

Speculation

The issue of whether the behavioral effects of left pulvinar damage in this patient are related to a sensory impairment that results in compensatory eye movement changes, or motor abnormalities (eye movements) that disrupt perception, is an intriguing but at this point unanswerable question. The known neuroanatomical connections and studies characterizing the electrophysiological properties of pulvinar neurons indicate that the posterior pulvinar could participate in both types of functions. For example, some pulvinar neurons discharge in association with eye movements to a visual stimulus, while others do so in the dark [27,30]. Similarly, the connections of the posterior region of the pulvinar include visual association cortex (sensory) as well as the frontal eye fields and the pretectum (see [S, 241) (motor). Systematic study in experimental animals is needed to confirm the present findings, to resolve the issue of direct parietal damage, and to investigate the sensory and motor nature of alterations in eye movement behavior following pulvinar lesions.

A~l\r~o~~/edyeme,lt.s The authors acknowledge R. P. MIUS, M.D., and A. FIK.HS, Ph.D.. for neuro-optllaimological assessment, and J. %hG for secretarial assitance. MPO was supported by the Dolly Green Scholar Award from Research to Prevent Blindness, Inc. to Dr. AYITA H~NDRICKSOZI. CAM and ARW are recipients of Teacher- Investigator Awards NS00505 and NSOO195 awarded by the National Institutes of Neurological and Communicative Disorders and Stroke, PHSiDHEW and are affiliates of the Child Development and Mental Retardation Center, Seattle. Equipment support was provided by NIH-BMRSC Grant SO7 RR05432 awarded to CAM.

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