Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey

1987 ◽  
Vol 57 (5) ◽  
pp. 1262-1287 ◽  
Author(s):  
M. R. Dursteler ◽  
R. H. Wurtz ◽  
W. T. Newsome

Ibotenic acid lesions of the middle temporal visual area (MT) have previously been shown to impair a monkey's ability to initiate smooth pursuit eye movements to targets moving in the extrafoveal visual field (30). This is a retinotopic deficit: pursuit is impaired in all directions within the affected portion of the contralateral visual field. In the present experiments we analyzed the effects of lesions of the foveal representation of MT on the maintenance of foveal pursuit. Injections of ibotenic acid were directed toward the representation of the fovea within MT but spread into extrafoveal regions of MT and adjacent visual areas within the superior temporal sulcus. Chemical lesions of the foveal representation produced a directional deficit in the maintenance of pursuit: the monkey failed to match eye speed to target speed when pursuing a target that moved toward the side of the brain with the lesion. This deficit was evident regardless of the part of the visual field in which target motion began, and pursuit at higher target speeds was more severely affected. The directional deficit was qualitatively similar to pursuit deficits observed in human patients following large parietal-occipital lesions. Extension of the lesions into extrafoveal regions of the contralateral visual field representation also resulted in retinotopic deficits for pursuit initiation: the monkey was unable to match the speed of its pursuit eye movement to that of a target or to adjust the amplitude of its saccade to compensate for target motion. The errors in pursuit speed and saccade amplitude for initiation of pursuit into the contralateral visual field were linearly related, which supports the hypothesis that both deficits arise from damage to the same underlying visual motion processing mechanism. The selectivity of the retinotopic deficit for motion information was also investigated by reducing retinal motion through the use of a stabilized image. After the lesion, the monkeys continued normal pursuit when a position error was present during stabilization, supporting the view that the deficit was related to loss of motion but not position information.

1988 ◽  
Vol 60 (3) ◽  
pp. 940-965 ◽  
Author(s):  
M. R. Dursteler ◽  
R. H. Wurtz

1. Previous experiments have shown that punctate chemical lesions within the middle temporal area (MT) of the superior temporal sulcus (STS) produce deficits in the initiation and maintenance of pursuit eye movements (10, 34). The present experiments were designed to test the effect of such chemical lesions in an area within the STS to which MT projects, the medial superior temporal area (MST). 2. We injected ibotenic acid into localized regions of MST, and we observed two deficits in pursuit eye movements, a retinotopic deficit and a directional deficit. 3. The retinotopic deficit in pursuit initiation was characterized by the monkey's inability to match eye speed to target speed or to adjust the amplitude of the saccade made to acquire the target to compensate for target motion. This deficit was related to the initiation of pursuit to targets moving in any direction in the visual field contralateral to the side of the brain with the lesion. This deficit was similar to the deficit we found following damage to extrafoveal MT except that the affected area of the visual field frequently extended throughout the entire contralateral visual field tested. 4. The directional deficit in pursuit maintenance was characterized by a failure to match eye speed to target speed once the fovea had been brought near the moving target. This deficit occurred only when the target was moving toward the side of the lesion, regardless of whether the target began to move in the ipsilateral or contralateral visual field. There was no deficit in the amplitude of saccades made to acquire the target, or in the amplitude of the catch-up saccades made to compensate for the slowed pursuit. The directional deficit is similar to the one we described previously following chemical lesions of the foveal representation in the STS. 5. Retinotopic deficits resulted from any of our injections in MST. Directional deficits resulted from lesions limited to subregions within MST, particularly lesions that invaded the floor of the STS and the posterior bank of the STS just lateral to MT. Extensive damage to the densely myelinated area of the anterior bank or to the posterior parietal area on the dorsal lip of the anterior bank produced minimal directional deficits. 6. We conclude that damage to visual motion processing in MST underlies the retinotopic pursuit deficit just as it does in MT. MST appears to be a sequential step in visual motion processing that occurs before all of the visual motion information is transmitted to the brainstem areas related to pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)


1989 ◽  
Vol 61 (1) ◽  
pp. 173-185 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko

1. The goal of our study was to determine the properties of the visual inputs for pursuit eye movements. In a previous study we presented horizontal target motion along the horizontal meridian and showed that targets were more effective if they moved across the center of the visual field. We have now analyzed the topographic weighting of the inputs for pursuit in greater detail, using targets that moved in all directions and across a wide area of the visual field. 2. Monkeys were rewarded for tracking targets that started at 48 positions in the visual field. The initial positions were spaced equally around 4 circles that were centered at the position of fixation and had radii of 3, 6, 9, and 12 degrees. Targets moved horizontally or vertically at 30 degrees/s. We measured the smooth eye acceleration in the first 80 ms after the initiation of pursuit, before there had been time for visual feedback to affect the position or velocity of the retinal images from the target. 3. For both horizontal and vertical target motion, there were major differences between the early and late intervals in the first 80 ms of pursuit. In the first 20 ms eye acceleration was largely independent of initial target position. In later intervals eye acceleration decreased sharply as a function of initial target eccentricity. The later intervals also showed a pronounced toward/away asymmetry such that the initiation of pursuit was more vigorous for target motion toward than for motion away from the horizontal or vertical meridian. 4. Comparison of the topographic organization of the middle temporal visual area (MT) with our data on pursuit suggests that the topography of cortical maps is smoothed when the visual signals are transmitted to the pursuit system. For example, the superior visual hemifield is underrepresented in cortical motion processing areas, but target motion in the superior and inferior visual hemifields is equally effective for the initiation of pursuit. 5. We investigated the directional organization of the visual inputs for pursuit by presenting targets that started at 6 degrees eccentric and moved in 16 different directions. Horizontal target motion always evoked larger eye accelerations than did vertical target motion. Target motion in oblique directions evoked intermediate values of eye acceleration. 6. Our data show two classes of variation in pursuit performance. First, some subjects showed ideosyncratic variations that were restricted to one hemifield or one direction of target motion. We attribute these variations to differences among subjects in the physiology of visual pathways.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (4) ◽  
pp. 953-968 ◽  
Author(s):  
L. Tychsen ◽  
S. G. Lisberger

We have used the initiation of pursuit eye movements as a tool to reveal properties of motion processing in the neural pathways that provide inputs to the human pursuit system. Horizontal and vertical eye position were recorded with a magnetic search coil in six normal adults. Stimuli were provided by individual trials of ramp target motion. Analysis was restricted to the first 100 ms of eye movement, which precedes the onset of corrective feedback. By recording the transient response to target motion at speeds the pursuit motor system can achieve, we investigated the visual properties of images that initiate pursuit. We have found effects of varying the retinal location, the direction, the velocity, the intensity, and the size of the stimulus. Eye acceleration in the first 100 ms of pursuit depended on both the direction of target motion and the initial position of the moving target. For horizontal target motion, eye acceleration was highest if the stimulus was close to the center of the visual field and moved toward the vertical meridian. For vertical target motion, eye acceleration was highest when the stimulus moved upward or downward within the lower visual field. The shape of the relationship between eye acceleration and initial target position was similar for target velocities ranging from 1.0 to 45 degrees/s. The initiation of pursuit showed two components that had different visual properties and were expressed early and late in the first 100 ms of pursuit. In the first 20 ms, instantaneous eye acceleration was in the direction of target motion but did not depend on other visual properties of the stimulus. At later times (e.g., 80-100 ms after pursuit initiation), instantaneous eye acceleration was strongly dependent on each property we tested. Targets that started close to and moved toward the position of fixation evoked the highest eye accelerations. For high-intensity targets, eye acceleration increased steadily as target velocity increased. For low-intensity targets, eye acceleration was selective for target velocities of 30-45 degrees/s. The properties of pursuit initiation in humans, including the differences between the early and late components, are remarkably similar to those reported by Lisberger and Westbrook (12) in monkeys. Our data provide evidence that the cell populations responsible for motion processing are similar in humans and monkeys and imply that the functional organization of the visual cortex is similar in the two species.


Brain ◽  
2021 ◽  
Author(s):  
Gaurav H Patel ◽  
Sophie C Arkin ◽  
Daniel Ruiz-Betancourt ◽  
Fabiola I Plaza ◽  
Safia A Mirza ◽  
...  

Abstract Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for the cortical networks pertinent to the understanding complex social situations—in social inference, a key component of social cognition, in schizophrenia. 27 schizophrenia participants (SzP) and 21 healthy controls watched a clip of the movie “The Good, the Bad, and the Ugly” while high resolution multiband fMRI images were collected. We used inter-subject correlation (ISC) to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS BOLD activity 1) relationship with the motion content in the movie, 2) synchronization with other cortical areas involved in the viewing of the movie, and 3) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in SzP by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in SzP.


1991 ◽  
Vol 66 (3) ◽  
pp. 651-673 ◽  
Author(s):  
D. S. Yamasaki ◽  
R. H. Wurtz

1. Ibotenic acid lesions in the monkey's middle temporal area (MT) and the medial superior temporal area (MST) in the superior temporal sulcus (STS) have previously been shown to produce a deficit in initiation of smooth-pursuit eye movements to moving visual targets. The deficits, however, recovery within a few days. In the present experiments we investigated the factors that influence that recovery. 2. We tested two aspects of the monkey's ability to use motion information to acquire moving targets. We used eye-position error as a measure of the monkey's ability to make accurate initial saccades to the moving target. We measured eye speed within the first 100 ms after the saccade to evaluate the monkey's initial smooth pursuit. 3. We determined that pursuit recovery was not dependent specifically on the use of neurotoxic lesions. Although the rate of recovery was slightly altered by replacing the usual neurotoxin (ibotenic acid) with another neurotoxin [alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)] or with an electrolytic lesion, pursuit recovery still occurred within a period of days to weeks. 4. There was a relationship between the size and location of the lesion and the recovery time. The time to recovery for eye-position error and initial eye speed increased with the fraction of MT removed. Whether the rate of recovery and size of lesions within regions on the anterior bank were related was unresolved. 5. We found that a large AMPA lesion within the STS that removed all of MT and nearly all of MST drastically altered the rate of recovery. Recovery was incomplete more than 7 mo after the lesion. Even with this lesion, however, the monkey's ability to use motion information for pursuit was not completely eliminated. 6. The large lesion also included parts of areas V1, V2, V3, and V4, but analysis of the visual fields associated with this lesion indicated that these areas probably did not have a substantial effect on recovery. 7. We tested whether visual motion experience of the monkey after a lesion was necessary for recovery by limiting the monkey's experience either by using a mask or by using 4-Hz stroboscopic illumination. In one monkey the eye-position error component of pursuit was prolonged to greater than 2 wk, but recovery of eye speed was not. Reduced motion experience had little effect on recovery in the other two monkeys. These results suggest that such visual motion experience is not necessary for the recovery of pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)


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