f Ml28 3932.88 s3.00+0 WI 19% Pergamon Press plc CHANGES IN SENSORY INATTENTION, DIRECTIONAL MOTOR NEGLECT AND “RELEASE” OF THE FIXATION REFLEX FOLLOWING A UNILATERAL FRONTAL LESION: A CASE REPORT CHARLES M. BUTTER,* STEVEN RAPCSAK,? ROBERT T. WATSON and KENNETH M. HEILMAN Department of Neurology, College of Medicine, University of Florida and Veteran’s Center, Gainesville, Florida, U.S.A. Administration Medical (Received 25 May 1987; accrpted 9 Decrmhrr 1987) Abstract-We recorded eye movements to and away from visual stimuli from a patient with left-sided neglect following a right frontal infarct in order to determine (a) whether and to what extent his neglect was due to sensory inattention and directional motor neglect and (b) whether he had difficulty suppressing inappropriate eye movements to visual stimuli (“release” of visual grasp) as his sensory inattention declined. In the first testing session, conducted 5 days following his stroke, he often failed to move his eyes when a stimulus on the left required a rightward eye movement, but he consistently moved his eyes to a stimulus on the right. Thus, he showed contralateral but not ipsilateral sensory inattention. Initially, he also was impaired in making leftward eye movements when right stimuli were presented. Thus, he also showed a directional motor neglect. In subsequent tests, his left-sided sensory inattention as defined above decreased, and was no longer present three weeks following his stroke, nor in a follow-up test conducted almost 6 months following this stroke. In contrast, his directional motor neglect, as defined above, was still present in the follow-up test. As his left-sided sensory inattention declined, his tendency to move his eyes incorrectly to stimuli on the left side (the side contralateral to his lesion) when these stimuli required eye movements to the right became stronger (“release” of visual grasp); he continued to show this strong tendency in the test conducted almost 6 months following his stroke. INTRODUCTION INVESTIGATIONS of frontal lobe lesions in animals and humans have disclosed both decreased responses (i.e. neglect) [ 1, 8, 9, 11, 16, 26, 28, 3 1, 33, 37, 381 and increased or “released” orienting responses to external stimuli [3, 13, 24, 251. It is not clear when or under what conditions these opposed effects of frontal lobe lesions appear. Furthermore, there have been few attempts to determine whether neglect following frontal lobe lesions is sensory, motor (i.e. hemispatial and directional akinesia), or both. A sensory basis of neglect is suggested by the finding that monkeys with unilateral frontal eye field lesions show a contralateral impairment of visual detection when detection is evaluated by responses that are not directed to the visual stimulus [28]. Evidence for sensory neglect following frontal lesions is provided *Address correspondence to: Charles M. Butter, Neuroscience Laboratory, 1103 E. Huron MI 48109. U.S.A. tDepartment of Neurology, University of Arizona Health Sciences Center, Tucson, Arizona, 533 St., Ann Arbor. U.S.A. by findings ofcontralateral inattention to sensory stimuli in humans with frontal lobe lesions [9. 161. On the other hand. evidence has also been presented for a motor component in neglect following frontal lesions in monkeys 1371; in addition, contralateral motor neglect has been described in patients with unilateral frontal lesions [S, 311. However, in only one study involving monkeys [37] and one with human subjects [l] have both sensory and motor aspects of neglect been investigated in the same subjects. Recently we had the opportunity to test a patient with unilateral neglect following a right frontal lesion in a situation where we recorded his eye movements to and away from visual stimuli. Thus, we could determine whether and to what extent his neglect was sensory, motor or both. and whether he had difficulty suppressing inappropriate eye movements to visual stimuli (“release” of visual grasp). Since we tested this patient on several occasions, we also had the opportunity to trace the time course of his deficits and thus further clarify the relationship between visual neglect and release of visual grasp. CASE REPORT The patlent -as a hi-yr old. right-handed man with 3 yr of college education. Hc had :I history of treated hypcrtcnaion. On 5 ‘?,‘Xh his couorkcrs noted that hc was hating dllliculty using his left hand. and hc &as ndmittcd to ;L local hospital. TNO day\ later. he was transl’errcd to the Gaines~illc VAMC for further euluation. He complained of some difficulty with 111sleft hand but denied other problems. Hi:, general physical examination was unremarkahlc. except for a blood pressure of 168,‘90. His neurological cwmination rcvcalcd that hc M;IS alert and oriented to person. place and time. He had Icft-sided neglect on letter cnnccllation and line hwction. Whereas he rehpvndcd to most visual. auditory and tactile stimuli presented on the left side. he showed extinctIon In all three modalities. Hc also showed poor visuospatlal ability as disclosed by hl\ dcl’cctlcedrawing. Whereas his propositional speech was intact. hc showed a marked lack of prosody m his speech. which was still e\idcnt when he was retested several days later. However. he was able to recognize emotional tone 111 the cwminer’s speech HIP recent and remote memarq were intact. His cramal nerves were normal except for a mild left l’acial weakness. Pain, tcmpcrature. Ilght touch and joint position sense on the left sue decreased. He had mild ~vcnhncss on the left side of the body. especially distally. which interfered with fine movements ol’the fingus. Ccrchcllnr tats and gait were normal. Alth<>ugh hiA rctlevcs were symmrtrlc. he had an extcnwr plantar re\ponw on the I&. Forced grasping was not prcscnt. When movcmcnt\ wcrc elicited to command. he showed wnc motoi pcrsveration ;)‘I ucll as imperslstence. I.ahoratory tests at admission were normal. except for mild leuhoc! to\i\ (13.000) His wakmg EEG \ho\\ed right-sided 4ouing in thr delta range. superimposed on :~lpha :icti\‘it>. .t computerized tomographic scan (CT) on the day ofadmisbion to the VAMC showed a hypodenae area m the @it prcfrontnl and premotor cortex. Including the frontal cyc field. and extendins slightly into the Sql\ian lisure. the motor &trip and adjxent postccntral grub (ace b’ig. I I. The postorlur parietal lobe and occipital lobe showed no ahnormnlitlcs. Another CT scan tnhcn .: daya later (;~ppro\imatol> 7 day> follo\ving his stroke) AXE unchanged Ilc \ho\\cdsr;ldu;ll impro\cmcnt in the ux oIhia I& hand and arm over the course of his ctak In the hospital: III\ METHOD In I,rmal tehtlng, eye movements \+t‘rc recorded wth Ap AgCI electrodea (Beckman) attached to the external canthl DC potentials were amplilied and rccordcd on ;I Grxa polygraph (7WC XPA). In the first testing session. conducted 3 Jaya fbllowing 111sadmission. the patlent N;!S imtiall) instructed to move hia eyes Cram a central lixation point (the examiner’, nose) to the eumincr’s left or right index linger (located approximately 30 laterally) w hen one of them moved (uncroshcd-reapon~~ tat). Nat. he was instructed to fixate the examiner’s nose and. when the cxamincr moved his ~ndc\ tingcr. to mobc his cycs to the wte opposite It and toward the index finger that was nol moving (crossed-rcsponx test). In three subsequent scssionh. conducted o\cr a l7-day period, the visual stunull ucrc pro\idcd hq two. 7X-V red-jeweled Lumps. located on a black pcrmwter. 30 tu the left and right of the center The lamps were I .1 cm in dumcter: at the Liewing distance employed they suhtcndcd I .3 During testing. he sit facing the perimeter with his chin in ;L molded alpport. In the first suits of trials (uncrossed-response test) he \\a Instructed to liuatc a small spot 111the c‘cntcr of the pwmetcr and to move III> cqcs to a lamp Nhcn it was hrlctlq illuminated (0.5 0.75 xc). After complctln, ~7tho lirst writa of trials. he \\a instructed to mole his eqcs rrom the lixation spot to the unilluminated lamp on the side opposite the one hrieny Illuminated (crosed-rcsponsc test ). In each scssiun stirnull wrc prexntcd IX 30 tlmeh in each of the two ux:, of trials, approximately 50” o on each hidc sec~uencc. .Approulmatcl) 6 months Inter. 1115QC In each sxich. stimuli \+erc prcscnted in ;I ~“‘~~dorand~,rn CHANGES IN SENSORY INATTENTION, DIRECTIONAL MOTOR F~ti. 1, CT scan at fibe levels showclng patient’s NEGLECT right frontal AND “RELEASE” infarct 535 CHANGES IN SENSORY INATTENTION. DIRECTIONAL MOTOR NtGLC(‘T ANIl “RELEASt” 537 movements were again recorded while he moved his eyes toward and away from tlluminated lamps by the same procedures used in the previous three sessions. The control subjects were fve men ranging in age from 53 to 66 yr (mean age=62 yr). They were free of neurological disease involving the brain and had no eye movement disorders. None had histories of alcohol or drug abuse. Their eye movements were recorded while they were tested in a single session by the same procedures employed with the patient in the last four sessions. In the uncrossed-response test, failure to move the eyes toward a stimulus contralateral to the lesion could be attributed either to sensory neglect or to directional motor neglect to or to both. However. in the crossed-response test. failure to mov’e the eyes when a stimulus is presented on the side contralateral to the lesion cannot be explained by motor neglect and indicates sensory neglect. Furthermore. when stimuli are presented ipsilateral to the lesion in the crossed-response test. failure to move the eyes away from the stimulus and into contralateral hemispace cannot be explained by sensory neglect and suggests directional motor neglect. Finally. in our test, release of visual grasp to a stimulus is indicted by initially moving the eyes toward the stimulus (even if it is followed by a correct eye movement to the right) in the crossed-response test. RESULTS Table 1 shows the two kinds of errors that the patient and his controls made in testing-incorrect eye movements and failures to perform eye movements-when they were presented with stimuli on each side in the uncrossed- and crossed-response tests. Whereas the control’s subjects made very few errors in any of the conditions of testing, the patient made considerably more errors in both the uncrossed and crossed-response tests. Furthermore, the severity of his impairments in some of the tests varied with the time of testing. With regard to his performance with the uncrossed-response tests, his total errors in moving his eyes toward left-sided stimuli (the side contralateral to his lesion), which provide a measure of his overall left-sided neglect, was 23.3% in the first session. In contrast, in the same session, his total errors in moving his eyes toward stimuli on the right side, which provide a measure of his overall right-sided neglect, was only 3.3% over the next three sessions, which spanned a 16-day period. A similar result was obtained when he was retested approximately 6 months after his stroke (see Table 1). With regard to his performance in the crossed-response tests, his total errors in moving his eyes to the side that he neglected (the left) in response to stimuli presented on the opposite side were substantial in the first two sessions (20.6 and 31 .O%). Although his total errors in this testing condition declined somewhat in sessions 3 and 4, in the final session they were as frequent as they had been in the first session. Second, when stimuli were presented on the left side in the crossed-response test of the first session, the patient’s failure to move his eyes, which assesses his sensory inattention to the left independently of his motor neglect, was evident in a large number of trials (38.7%). Over the next three sessions, the frequency with which he failed to perform eye movements in this testing condition declined and was zero in the final session (see Table 1). Thirdly, whereas initially. the patient made very few incorrect eye movements to stimuli presented on the left side in the crossed-response test; in subsequent sessions his tendency to inappropriately move his eyes to left-sided stimuli grew stronger until, in the final session, he did so on more than 80% of the trials. On most of the trials in which he made these errors, he performed corrective saccades to the right. In contrast to his increasing tendency to look toward left-sided stimuli in the crossed-response tests, his tendency to inappropriately move his eyes toward stimuli presented on the right side in the crossed-response tests. which varied between 10 and 23%, did not increase over the five testing sessions (see Table I). The patient’s deficit in moving his eyes to the left when right-sided stimuli were presented in early testing sessions was accompanied by other eye movement deficits. When DC (&I!S Te51 follo\ring Cro\\ed-rciponw ~:ncro~~ed-respol~s~ Se\slon 10.3 20 (0 5.0) R PT. (‘ant 3.7 2.0 (0 5.0) 1. PT. <‘ant. 10.3 0 38 7 0 33 I .o (0 5.0) 0.0 0.0 0.0 0.0 Cant “4,x ” F.M. R PT. Cont. I (5) X.0 “/,,Incorr KM. 3.3 Slim. poution 2 (I?) 33.0 12.5 55 0.0 x.0 12.5 5.5 16.0 % No E.M. 10.0 37.9 0 3.7 1.3 13.x 0 15.1 subjects II.1 75.0 4.5 0.0 -- __^-._I”__ 0.0 5.0 9.1 9.5 4 (21) “%>No ‘/i,Incorr E.M. E.M. (PT.) m each scs~ion and control 3 (14) “Alncorr “/“NO E.M. E.M. (Ko. E.M.)* of patlent ‘J~~Ilncorr E.M. ~ncorrcct (Inc. E.M.) and no eye mo\emcnt L PT. mol\eJ -Table I, Pcrccnl 20.0 81.2 0 0 _ 0.0 0.0 7.1 6.2 5 (170) %lncorr %IN o E.M. E.M. (Cont.)t -J v 2 c 5 W 2 : r: F CHANGES IN SENSORY INATTENTION, DIRECTIONAL MOTOK NEGLK’T AN11 “RELtASE” 539 amplification was sufficient to evaluate saccade amplitudes (sessions 1 and 3), he showed hypometric eye movements to the left. In session 1, the mean amplitude of his correct leftward saccades (X= 20.7”) was significantly smaller (t = 6.03; df= 90; P~O.005) than the mean amplitude of his rightward saccades (X= 27.7”), which was close to the eccentricity of the target (30”). A similar result was obtained in session 3 (mean amplitude of correct leftward saccades = 23.4”; mean amplitude of correct rightward saccades = 28.7’; t = 4.38; clf=Xl; P-cO.0005). Furthermore, similar differences between leftward and rightward saccades were also found on both uncrossed and crossed-response trials in these sessions (P. 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