Troubled reaching after right occipito-temporal damage

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Vol. 30, No. R, pp 711 722. 1992 Rnta~n.

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0028 3932, Y2 $5 OO+O.oO 1992 Pergamon Pm\ LLd

AFTER RIGHT OCCIPITO-TEMPORAL DAMAGE

MATTHEW RIZZO,* DIANE ROTELLA+ and WARREN DARLING? *Department of Neurology

and tDepartment

(Rrceired

30

of Exercise Science, The University Iowa. U.S.A.

September 1991:

accepted

9 March

of Iowa, Iowa City,

1992)

Abstract-We

encountered a man with an unusual reaching disturbance due to a stroke in the right occipito-temporal cortex and subjacent white matter. We studied his behavior in detail including vision and hand control. He had a left homonymous hemianopia. In his remaining fields static visual acuity and stereoacuity were normal, but he could not detect a coherent motion signal or follow moving targets with smooth pursuit. Transduction of limb movements using an optoelectronic technique showed abnormal morphology, increased variability and markedly prolonged latencies for transport to external visual targets, yet he achieved these targets with precision. Reaching to selfbound targets, and to the remembered locations ofexternal targets with vision blocked was 5 x faster. The findings may be explained by: (1) damage in regions homologous to areas TF and TH in the monkey, which provide visual inputs to hand and forelimb representations in the cortex; (2) injury in human regions homologous to the monkey’s MT complex, with inability to use visual information on the movement of the limb due to a visual motion processing defect; and (3) disruption of visual cortical subcortical connections mediating crucial transformations among limb and target representations.

INTRODUCTION VISUALLY-GUIDED reaching to objects in extrapersonal space is a task crucial to man’s existence and normal functioning. To succeed, the brain must (1) transform a target’s visual coordinates to body-centred space and specify the necessary limb-segment orientations for target acquisition; (2) plan a hand trajectory and velocity (which involves the specification of multiple joint torques); and (3) activate appropriate muscle groups to meet those specifications. How the brain rapidly solves these difficult control problems remains an important research question. Microelectrode and ablation studies 119, 261 have begun to define a neural substrate for reaching movements in monkeys, although evidence in the human emerged first. In 1909 BALINT [2] described optic ataxia, in which brain-damaged subjects may grope as if blind for targets under visual guidance, yet point with precision on their own body. More recent studies on the topic stress the role of the visual association cortex in the occipito-parietal regions, although the evident complexity of normal reaching suggests other structures may also be involved [ 17, 231. We encountered a man with a reaching disturbance that in some respects resembled optic ataxia. Yet the impairment in this unusual case was due to a lesion in the occipito-temporal

*Address correspondence to: Dr Matthew Rizzo, Department of Neurology, The University and Clinics. Iowa City, Iowa 52242, U.S.A. Tel.: (319) 356-8755; FAX: (319) 356-4505. 711

of Iowa Hospitals

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MATTHEW R~rro,

DIAZ~ ROTELLA and WAKKEN DAKLING

cortex and subjacent white matter rather than to an occipito-parietal lesion. The purpose of this study was to characterize such a defect with respect to a putative neural substrate for reaching. To do so we studied the patient’s behavior in detail. including aspects of handmovement control. This employed a system which allows quantitative three-dimensional (3-D) recordings of limb trajectory, timing, and accuracy through infrared transduction of movement patterns.

METHOD Suhjl!c7 The subject was a 60.year-old right-handed man who suffered a thromboembolic stroke of the right hemisphere that included the visual association cortex in an occipito-temporal location and the subcortical white matter near the pulvmar (see Fig. I ). Thereafter his chronic problems included: (I ) a severe reaching disturbance especially with the left hand, and (2) associated deficits of visual perception. Before the ictus he had no problema with \ ision or hand movements. no movement disorder (including Parkinson’s disease). and performed his dally activities without difficulty. Salient findings included no tremor. rigidity, masked facies. postural instability or gait abnormalit). Rapid alternating movements were symmetrical. He had no weakness to explain his reaching behavior. Under cycsclosed conditions he showed no pronation or drift of the outstretched arms and could accurately report displacements in his finger. wrist, elbow and shoulder joints made by the exammer. Neuro-ophthalmological examination showed no eye abnormalities to account for his defect. Visual acuity wah 20:20 OU with correction. GOLIIMANP;perimetry [I] showed a left homonymous hemianopia. Static stereoacuitl was normal at 40 set of arc (Randot, Stereo Optical Co.. Chicago, undated). Visual motion perception was tested on a modified version of the random dot cinematogram (RDC) paradigm of BLFFIYGTON et ul. 177 (see also NEWSOME and PAKE 1281). This procedure used computer-controlled animation sequences depicting a cluster of200 randomly spaced black dots moving against a white background. On each trial a given proportion of the dots (the “signal” dots) moved in one consistent direction. The remainder (the “noise dots”) changed direction at random, The subject’s task was to report the direction of flow (up, down, right or left) of the resultant coherent motion signal. He failed this at several different speeds (from 2 to IO set). We also asses~d whether he could track moving targets with smooth-pursuit eye movements. The target was a small (0.25 1 suprathreshold light movingacross the face ofan HPl300A cathode-ray display at 9, I5 or 25 see.These triangularwave excursions spanned I5 horizontally. Magnetic search coil recordings (Skalar, Delft. resolution I min) showed that the resultant pursuit eye movements were mostly saccadic. Neuropsychological assessment showed defective vlsuospatial processing in the subject.5 remaining fields based on abnormal three-dlmensional block design, and poor reproduction of line drawmgs to copy (Rey Osterreith Jand from memory (Benton VRT). He sometimes failed to report external objects on his left despite unrestricted viewing opportunities. and would occasionally fail to report touch on his left to double simultaneous tactile stimulation. He was aware of his reaching defect and it distressed him. Language and memory were intact outside of vision.

Neurological observations were videotaped. On reaching for fixed targets at arms length with the left hand the subject would first turn his head toward a target and fixate it. Once he had the object in Liew hc extended the limb very deliberately, looking back and forth between his hand and the target through final acquisition. He was extremely slow to achieve targets on either side of midline. The problem was much less evident with the right hand. We quantified these results using the apparatus and technique dcscrlbed below.

Targets consisted of four highly visible yellow markers (dia. I .3 cm) mounted on a black matte table surface (measuring 60 x 45 cm). A start position target was located directly in front of the subject m the midllnc. The remaining targets were each 35 cm distant from the start position with the middle target being directly anterior and the left and right targets I5 cm to either side of it. The subject was comfortably seated at the table so that the start and middle targets were in line with his midline. Head and hand movements were not restricted in any way. WC evaluated the ability to smoothly transport each hand from the start position. to touch with the index finger the right, left or middle target. and then return. Ten “roundtrips” were made with each hand to each target. The subject wab tested with the eyes open (a “closed loop” condition allowing visual feedback on the reaching Itmh), and with vision blocked. In the latter procedure. movements to the subject’s nose (Intrinsic target) and return movements to an external target (starting position) were tested with eyes closed. Control subjects included five individuals with unilateral cerebral damage and no reaching disturbance (three with homonymous hemianopia comparable to the target subject‘s). one with bilateral cerehellar Icsions. and tw’o 65. year-old normal control subjects without brain lesions.

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Fig. I. Analysis of MRI data followed a standard neuroanatomtcal technique [Xl. Coronal plots show the right hemisphere lesions in the target patient m black. The damage affected the right mesial infracalcarine and antero-mesial supracalcarinc regions (in the white matter), mesial occipitotemporal junction (extending deep into white matter surrounding the postero-lateral thalamus), parahippocampal and fourth temporal gyri. and hippocampus.

Data acquisition relied on an optoelectronic technique. Infrared emitting diodes (IREDS) were placed on the nail ofcach index finger and on the forehead, Their positions were recorded by two i.r. cameras (WATSMART system, Northern Digital). Prior camera calibration using a three-dimensional frame and direct linear transformation software allowed accurate determination of the three-dimensional spatial coordinates of the body mounted IREDs. IRED position were digitized at from 50 to 200 Hz for up to 20 SK. depending on hand-movement speeds. All movement trials were inspected to exclude reflection artifacts or other sources oferror. Plots of movement positton and speed of the fingertip could then be extracted from the smoothed (IO Hz low pass Butterworth digital filter, zero phase shift) digitized data to determine movement onset and endpoints from velocity thresholds. Movement onsets and endpoints for the target patient were determined by visual analysis of position records.

RESULTS Figure 2 shows the path taken by the left hand, viewed from above, to targets on the left, middle and right. The 65year-old normal control subject (see Fig. 2(b)) made smooth, and

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Fig. 2. Paths of fingertip movements skewed from above to targets (open circles) on the left. middle and right. All movements began from the same position just anterior to the subject. The subjects had unrestricted view of the external targets and visual feedback from the reaching arm. a “cloacd-loop” condition. The paths of ten movements to each of the three targets are superimposed. (a) The paths of the left fingertip of the target subject are shown. (b) Fingertip paths in a 65-year-old normal control subject.

almost straight movements to each target. By contrast the patient’s hand movements (see Fig. 2(a)) were extremely slow and appeared to consist of a series of small submovcments. This is shown in Fig. 3(aad) which shows hand position (lower traces) and velocity (upper traces) along the anatomical A-P axis (ordinate) for movements towards the middle target. Note the different time scales on the abscissa. The movement durations by the target patient (Fig. 3(d)) averaged nearly 9 set compared to only 1.5 set in a patient with a severe truncal and appendicular dystaxia due to a cerebellar syndrome (Fig. 3(b)), 0.6 set in a subject with left homonymous hemianopia (Fig. 3(c)), and 0.7 set in the 65-year-old control (Fig. 3(a)). Indeed, the target patient made left hand movements that averaged about IO x those of all other patients and normal controls (Fig. 4(b)). Interestingly, his right hand movements were also abnormal since movement durations were about two-fold increased (Fig. 4(a)). His hand movements were “discontinuous” in the terminology of BROOKS et al. [6] based on velocity records which showed multiple peaks (Fig. 3(d)), in contrast to the normal and brain-damaged control subjects (except for the cerebellar patient) who moved smoothly and showed one major velocity peak (Fig. 3(b)). As an indication of movement accuracy. we calculated endpoint variability of the movements as the area of an ellipse with radii equal to I SD in the medial -lateral and anterior-posterior directions at the time of movement termination 1161. Accuracy of the movements by the target patient was quite good, as indicated by the low endpoint variability in comparison to other patients and controls (Fig. 5). Thus, despite great difficulty. this patient was eventually able to achieve the desired target. Figure 6 shows reaching with vision blocked. These movements began after the subject’s left index finger was placed by the examiner at the distal midline yellow marker. Subsequently he made movements toward his own nose (Fig. 6(a)), then back (Fig. 6(b)) to

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Fig. 3. Time-course ofpositlon (lower traces) and velocity (upper traces) for hand movements toward the middle target made by a 65-year-old normal control subject (a). a cerebella patient (b). a control patient with left homonymous hemianopia (c), and the target patient (d). The records of 8 IO movements are superimposed on each of (a), (b). (c)and (d). Note the different tm~c-xxlca. Vision IS unrestricted as in Fig. 2.

the remembered target location (a variant of an “open-loop” condition, since the subject is reaching for the external target without visual feedback on limb position). Notably. these 60 cm reaches take 3-5 x less time than the 35 cm (“closed loop”) reaches shown in Fig. 3!b), despite the extra distance they cover. Furthermore the velocity tracings in Fig. 6 are continuous, not discontinuous.

DISCUSSION The results of this study provide a clear description of the defective reaching movements in the target subject. The salient findings include abnormal movement morphology, increased spatio-temporal variability during the transport phase, and markedly prolonged latencies to target, especially under visual guidance and with the left hand. These defects followed a

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Fig. 3. Durations of right-handed (a) and left-handed (b) movements tu the three targets b> iill subjecta. Vision is unrestricted as in Fig. 2. The bars show mean movement duration for the target patient. brain-damaged controls (f?-6) and normal control subjects (r1=2). The error bars iire the mwn ofthe within-subjects standard deviation 111movement duration and. thuh. represent \arlabilit! in movcmcnt duration.

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Fig. 5. Variability at movement endpoint for right-handed (a) and left-handed (b) movements to all three targets by all subjects. Vision is unrestricted as in Fig. 2. The bars show mean endpoint variability of 8-10 movements (defined as the area of an ellipse with radii equal to I SD in the anterior-posterior and medial lateral directions at the time of movement termination) for the target patient. brain-damaged controls ()I= 6) and normal controls (?I= 2). The error bars represent the standard error of the mean of the endpomt variabilities of all subjects in each group.

Fig. 6. Time-course of position (lower traces) and velocity (upper traces) for several reaches with vision blocked. After positioning the subject’s left index finger was placed by the examiner at the distal midline yellow marker, the target patient made 60 cm movements toward his own nose (a). and back (b) to the remembered target location (a version of an “open-loop” condition since the subject is reaching for the external target without visual feedback on limb position). These movements take 4 5 x less time than the 35 cm (“closed loop”) reaches depicted m Fig. 3(b). despite the extra distance. Furthermore, the velocity tracings are nearly continuous. rather than discontinuou\.

stroke in the right hemisphere which damaged the occipito-temporal regions and the subjacent white matter (see Fig. 1). The abnormal reaching in this case was not due to impaired joint position sense. weakness or Parkinson’s disease. The patient also had no evidence of structural damage in the basal ganglia or cerebellum. His reaching differed from that in cases of homonymous hemianopia (Fig. 3(c)), and in a patient with cerebellar damage. The latter exhibited intention tremor with corresponding velocity changes as expected (see Fig. 3(b)), and unlike the target patient did not exhibit such prolonged movements. While the target patient did show some evidence of neglect of objects in left visual space. this condition does not explain why he also had severe trouble reaching to the midline and right; that he recognized his left arm, its trouble, and still used it, militate against motor neglect. Cornparisor~

\clith optic

atasia

In several respects the abnormal reaching movements in this subject resembled optic ataxia, being defective under visual guidance, worse with the contralateral hand, and worse to the extrapersonal space contralateral to the lesion [ 15. 171. He also showed greater facility with hand movements to self-bound targets. But clearly he did not “grope” under visual guidance [l I] as has been emphasized in optic ataxia. On the contrary, the endpoint variability of his movements, an index of accuracy to visual targets, was comparable to that of the two normal 65-year-old controls, and of other brain-damaged subjects who had no clinically evident reaching disturbance. Moreover the posterior parietal and parietooccipital areas (e.g. 5. 7 and 39, and superior 19). regions of reputed importance for optic ataxia [ 1 l] were spared. The deficits in this case merit further consideration in light ofcurrent concepts on hand control.

Anutotnophysioloyi~

considerations

Reaching depends on complex transformations among target and limb coordinates. In a transport phase the hand is moved toward an object whose position is determined by vision or memory. In an acquisition phase, grasp formation depends on somatosensory and visual information on the limb and target 1221, familiarity with the target and, perhaps, predetermined motor programs. These phases mature at different rates, may be controlled independently before becoming coordinated [ 13, 34, 401, and can be dissociated by focal brain lesions [S]. Posterior parietal damage may affect neurons coding eye position in the head and stimulus location on the retina, which together with neurons in motor and premotor cortex permit hand movements to visual targets in a body-centred coordinate system 131. The schema proposed by SOECHTING and FLANDERS [33] takes origin at the shoulder, is closely related to the representation of object position and motion, and should depend on the visual cortex and its connections to other sensory and motor maps. TF, TH, hand andji~relitnh

control

The reaching deficits in our subject followed damage in the right occipito-temporal cortex and subjacent white matter. This should correspond, at least in part, to areas TF and TH in ths monkey 1391, and the connections to and from such regions. TF and TH project via several paths, including the cingulum bundle, to areas 24c and 23c (located in the depths of the cingulate sulcus) [25]. The latter areas each have a hand and forelimb representation. project to the cervical enlargement, and have corticospinal projections. Both are reciprocally connected to the forelimb representations of Ml and MII. It appears that 24c in particular may represent MI11 (personal communication, Gary W. Van Hoesen), a third motor representation concerned with getting the body stationed and ready for a distal movement controlled more by MI and MII. The damage in our patient would have disrupted critical inputs to homologous human representations. Such damage would probably lead to abnormal reaching, grasping and shaping movements of the hand prior to target acquisition. Vi.suul motion

perception

and lit& utntrol

It is important to consider that our patient had abnormal motion vision. He could not detect a coherent motion signal among noise in random dot cinematograms and made abnormal smooth pursuit eye movements. These findings resemble the results in other subjects [24,37,38,41] with lesions in a putative human homolog of the monkey’s area MT, a key unit in a neural network for motion. Moreover, the reaching deficits we describe resemble those reported by ZIHL c’t al. in a different “motion blind” subject [41]. That subject complained “I cannot follow my finger with my eyes if I move the finger too fast”, made corresponding slow hand movements under visual guidance, and like our subject performed better in an “open loop” condition, with vision blocked. Considering the apparent association between defective motion vision and defective limb control under visual guidance, it is logical to suppose that area MT participates in a neural network for the guidance of limb movements which overlaps the one for motion vision. The known anatomical relationships of area MT appear to be compatible with this hypothesis. Located in the depths of the superior temporal sulcus of the monkey, area MT belongs to a complex of neighboring cortical regions, namely MST, FST and VIP [4, 361. (The functions of the latter two areas are not well known, but they too are likely to be motion concerned.) This MT complex communicates with cortical areas Vl, V3, V4, TF and TH, and shares

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MAT~HLW RIZZO. DIANL ROTELLA and WAKKFY DAKLIX;

heterotropic connections with areas V2 across the callosum [lo, 14, 303. Moreover, it connects reciprocally with the frontal-eye field complex, parietal lobe (area PO), head of the caudate, superior colliculus, pulvinar, dorsolateral pontine nucleus and cerebellum [4, 8, 9, 361, all of which receive visual inputs mediating the control of eye, head, limb and body movements in extrapersonal space. The subject of ZIHL et al. [41,42] had intracranial venous sinus thrombosis, a condition which may cause extensive brain damage due to hemorrhagic infarctions and increased intracranial pressure [20]. Consequently she had bilateral cerebral lesions in structures which probably correspond to several portions of the neural networks outlined above. These lesions affected the visual cortex, optic radiations, and more anterior regions and connections in both hemispheres. They also affected the cerebellum [42], a critical structure for motor control that is also concerned with “higher function” [32] and with the processing of visual motion [21, 271. By contrast, our subject had focal circumscribed ischemic damage in the distribution of the posterior cerebral artery on the right, which spared the cerebellum and caused only unilateral cortical damage. His right occipito-temporal lesion (see Fig. 1) should have damaged a putative human MT complex (or at least afferent connections to it). The resultant motion vision defect, together with his other visuospatial processing impairments, probably altered his ability to code visual information on limb movement, and to correlate it with other maps of hand and target position. Disruption

of visual

cortical-suhcorticul

connections

Finally, we note that pathways for visual motion analysis, and for eye, head, limb and body control, include important connections from the visual cortex to subcortical stations [31]. In this vein, the white matter lesion in our patient may have disrupted occipitotemporal projections (including those from a putative human area MT) that normally reach the head and tail of the caudate nucleus and other motor-concerned portions of the basal ganglia [35, 391. This would help explain the observed bradykinesia under visual guidance. The lesion probably also disrupted projections to the pulvinar and superior colliculus. Both structures are important for mapping inputs among different modalities, including the somatosensory and visual association cortices [29]. Due to the destruction of fibers around the posterolateral thalamus, the outflow of the pulvinar was probably affected too. This would deprive the visual association cortex and basal ganglia of important connections pertinent to limb and target position, having perhaps an effect similar to pulvinar damage. Pulvinar lesions are not common in humans, but in the monkey are known to cause complex visuoperceptual and attentional defects that impair the localization of objects in visual space. Acknorrledyrments~This work was supported by NlH PO NS19632. We thank Dr Hanna Damasio for her analysis of the neuroimaging data, Drs Gary W. Van Hoesen and Kathleen Rockland for their insights on the corresponding nonhuman primate anatomy, and Dr Mark Nawrot who developed our motion vision paradigm.

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