Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate

1. To determine the possible role of the primate pretectal nucleus of the optic tract (NOT) in the generation of optokinetic and smooth-pursuit eye movements, we recorded the activity of 155 single units in four behaving rhesus macaques. The monkeys were trained to fixate a stationary target spot during visual testing and to track a small moving spot in a variety of visual environments. 2. The majority (82%) of NOT neurons responded only to visual stimuli. Most units responded vigorously for large-field (70 x 50 degrees) moving visual stimuli and responded less, if at all, during smooth-pursuit eye movements in the dark; many of these units had large receptive fields (greater than 10 x 10 degrees) that included the fovea. The remaining visual units responded more vigorously during smooth-pursuit eye movements in the dark than during movement of large-field visual stimuli; all but one had small receptive fields (less than 10 x 10 degrees) that included the fovea. For all visual units that responded during smooth pursuit, extinction of the small moving target so briefly that pursuit continued caused the firing rates to drop to resting levels, confirming that the discharge was due to visual stimulation of receptive fields with foveal and perifoveal movement sensitivity and not to smooth-pursuit eye movements per se. 3. Eighteen percent of all NOT units ceased their tonic discharge in association with all saccades including the quick phases accompanying optokinetic or vestibular nystagmus. The pause in firing began after saccade onset, was unrelated to saccade duration, and occurred even in complete darkness. 4. Most (90%) of the visual NOT units were direction selective. They exhibited an increase in firing above resting during horizontal (ipsilateral) background movement and/or during smooth pursuit of a moving spot and a decrease in firing during contralateral movement. 5. The firing rates of NOT units were highly dependent on stimulus velocity. All had velocity thresholds of less than 1 degree/s and exhibited a monotonic increase in firing rate with visual stimulus velocity over part (n = 90%) or all (n = 10%) of the tested range (i.e., 1-200 degrees/s). Most NOT units exhibited velocity tuning with an average preferred velocity of 64 degrees/s.(ABSTRACT TRUNCATED AT 400 WORDS)     

Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque

1. The anatomical connections of the dorsolateral pontine nucleus (DLPN) implicate it in the production of smooth-pursuit eye movements. It receives inputs from cortical structures believed to be involved in visual motion processing (middle temporal cortex) or motion execution (posterior parietal cortex) and projects to the flocculus of the cerebellum, which is involved in smooth pursuit. To determine the role of the DLPN in smooth pursuit, we have studied the discharge patterns of 191 DLPN neurons in five monkeys trained to make smooth-pursuit eye movements of a spot moving either across a patterned background or in darkness. 2. Four unit types could be distinguished. Visual units (15%) discharged in response to movement of a large textured pattern, often in a direction-selective fashion but not during smooth pursuit of a spot in the dark. Eye movement neurons (31%) discharged during sinusoidal smooth pursuit in the dark with peak discharge rate either at peak eye position or peak eye velocity, but they showed no response during background movement or during other visual stimulation. These units continued to discharge when the target was extinguished (blanked) briefly, and the monkey continued to make smooth eye movements in the dark. The majority (54%) of our DLPN units discharged during both smooth pursuit in the dark and background movement while the monkey fixated. Blanking the target during smooth pursuit revealed that these units fell into two distinct classes. Visual pursuit units ceased discharging during a blank, suggesting that they had only a visual sensitivity. Pursuit and visual units continued to discharge during the blank, indicating that they had a combined oculomotor and visual sensitivity. 3. Ninety-five percent of the units that discharged during smooth pursuit were direction selective. These units had rather broad directional tuning curves with widths at half height ranging from 65 to 180 degrees. Many preferred directions for DLPN units were observed, although the vertical and near-vertical directions predominated. 4. Most units that responded to large-field background movement were direction selective. During sinusoidal movement of a large-field background, half of them also discharged in relation to stimulus velocity, whereas others did not.     

Role of the pretectal nucleus of the optic tract in short-latency ocular following responses in monkeys

When a large-field image is suddenly moved in front of an observer, an ocular following response (OFR) with short latency (<60 ms in monkey and <85 ms in human) is observed. Previous studies have shown that neurons in the pretectal nucleus of the optic tract (NOT) of the monkey respond to movements of large-field visual stimuli. To understand the potential role of the NOT in the OFR, we first recorded single-unit activity in the NOT of four monkeys (Macaca fuscata). Sixty-six NOT neurons preferred large-field ipsiversive visual motion. In 86% (49/57) of the neurons, optimal directions were distributed over +/-30 degrees from ipsilateral. NOT units were sensitive to the speed of the visual motion; 54% (27/50) preferred slow (< or =20 degrees/s), 22% (11/50) preferred fast (> or =80 degrees/s) and the remainder intermediate speeds. Their response latencies to the moving visual scene were very short (approximately 51 ms), and 44% of them led the onset of the OFR by 10 ms or more. To characterize the response properties of these neurons, we reconstructed the temporal firing patterns of 17 NOT neurons, using the acceleration, velocity, position and bias components of retinal image slip or eye movements during the OFR by a least squares error method. For each stimulus speed fitting condition, using either retinal slip or eye movements, their firing patterns were matched to some extent although the goodness of fit was better using retinal slip than when eye movements were used. Neither of these models could be applied independently of stimulus speed, suggesting that the firing pattern of the NOT neurons represented information associated with retinal slip or eye movements during the OFR, over a limited range. To provide further evidence that the NOT is involved in generating the OFR, we placed unilateral microinjections of muscimol into the NOT. Following the muscimol injection, we observed a approximately 50% decrease in eye velocity of the OFR toward the side of injection regardless of stimulus speed, while only a weak effect was observed in the OFR during contraversive or vertical image motion. These results suggest that the NOT may play a role in the initiation and support of the short-latency ocular following response.     

Visual motion response properties of neurons in dorsolateral pontine nucleus of alert monkey

1. In this study we sought to characterize the visual motion processing that exists in the dorsolateral pontine nucleus (DLPN) and make a comparison with the reported visual responses of the middle temporal (MT) and medial superior temporal (MST) areas of the monkey cerebral cortex. The DLPN is implicated as a component of the visuomotor interface involved with the regulation of smooth-pursuit eye movements, because it is a major terminus for afferents from MT and MST and also the source of efferents to cerebellar regions involved with eye-movement control. 2. Some DLPN cells were preferentially responsive to discrete (spot and bar) visual stimuli, or to large-field, random-dot pattern motion, or to both discrete and large-field visual motion. The results suggest differential input from localized regions of MT and MST. 3. The visual-motion responses of DLPN neurons were direction selective for 86% of the discrete visual responses and 95% of the large-field responses. Direction tuning bandwidths (full-width at 50% maximum response amplitude) averaged 107 degrees and 120 degrees for discrete and large-field visual motion responses, respectively. For the two visual response types, the direction index averaged 0.95 and 1.02, indicating that responses to stimuli moving in preferred directions were, on average, 20 and 50 times greater than responses to discrete or large-field stimulus movement in the opposite directions, respectively. 4. Most of the DLPN visual responses to movements of discrete visual stimuli exhibited increases in amplitude up to preferred retinal image speeds between 20 and 80 degrees/s, with an average preferred speed of 39 degrees/s. At higher speeds, the response amplitude of most units decreased, although a few units exhibited a broad saturation in response amplitude that was maintained up to at least 150 degrees/s before the response decreased. Over the range of speeds up to the preferred speeds, the sensitivity of DLPN neurons to discrete stimulus-related, retinal-image speed averaged 3.0 spikes/s per deg/s. The responses to large-field visual motion were less sensitive to retinal image speed and exhibited an average sensitivity of 1.4 spikes/s per deg/s before the visual response saturated. 5. DLPN and MT were quantitatively comparable with respect to degree of direction selectivity, retinal image speed tuning, and distribution of preferred speeds. Many DLPN receptive fields contained the fovea and were larger than those of MT and more like MST receptive fields in size.(ABSTRACT TRUNCATED AT 400 WORDS)     

Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions

Summary The response properties of cells in the lateral (LTN) and dorsal (DTN) terminal nuclei of the accessory optic system (AOS) were examined in 14 cats which underwent unilateral visual cortex ablation. Following decortication, single units in the LTN and DTN no longer showed the high degree of binocular convergence characteristic of the intact animal, but instead LTN and DTN units became almost completely dominated by the contralateral eye. In addition, responsivity of LTN and DTN cells to high stimulus velocities was abolished by removal of cortical input. This decrement in high velocity response was observed in both the excitatory and the inhibitory components of the velocity response profile.While the incidence of direction selective neurons in both the LTN or the DTN was not affected by decortication, the distribution of preferred and non-preferred directions was dramatically altered in the LTN, and to a lesser extent in the DTN. In the LTN, there was a severe reduction in the number of cells which displayed maximal excitation for upward stimulus motion. Instead, most LTN units in the decorticate cat preferred downward directed stimulus motion. In the DTN, most units still preferred horizontal stimulus motion as in the intact animal, but the overall distribution of preferred directions displayed a clear downward vertical vector component. In other respects, such as receptive field size and position in visual space, on/off responses, and resting discharge rate, LTN and DTN units appeared unaffected by cortical lesions.These experiments demonstrate that the cortical input to the LTN and DTN plays a highly significant role in the formation of response properties of cells located in these nuclei. The results presented in this report indicate that the visual cortex is a major source of ipsilateral eye input, high velocity responses, and upward direction selectivity for the AOS units examined in these experiments.     

Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system

Visual responses were examined quantitatively in 96 units in the lateral (LTN) and dorsal (DTN) terminal nuclei of the cat accessory optic system (AOS). The receptive fields of LTN and DTN cells were quite large, with an average diameter of approximately 60 degrees. Individual cell receptive fields, which could be as small as 30 degrees vertically by 15 degrees horizontally or as large as 100 by 100 degrees, always included the area centralis. Large, moving textured stimuli provoked optimal modulation in these cells. In response to a 100 by 80 degrees random-dot pattern moving at a constant velocity, nearly all cells in both the LTN and DTN displayed a high degree of direction selectivity. Directional response profiles were subjected to a vector analysis that generated two quantities proportional to the direction and magnitude of the major excitatory (E vectors) and inhibitory (I vectors) responses of individual cells. Directional vectors of the LTN displayed a strikingly bimodal distribution: E vectors of individual LTN cells pointed either upward (25 of 49) or downward (23 of 49). I vectors also pointed either up or down in a direction opposite to that of the E vector for the same cell. E and I vectors in both LTN and DTN units were separated by approximately 180 degrees. With few exceptions, E vectors of DTN cells pointed in a horizontal-medial direction, while DTN I vectors pointed in a horizontal-lateral direction. A relatively broad range of stimulus velocities (0.8-102.4 degrees/s) evoked maximal excitation in individual LTN units. The majority of LTN cells, however, achieved maximal excitation at velocities between 0.8 and 12.8 degrees/s. The deepest inhibition was elicited over a range of velocities from 0.2 to 102.4 degrees/s, with two major peaks at 0.8 and 12.8 degrees/s. A similar range of velocity sensitivity was observed in DTN cells: maximal excitation was obtained for stimulus velocities from 1.6 to 102.4 degrees/s, with most DTN cells showing the greatest excitatory response between 6.4 and 12.8 degrees/s. A broad range of inhibitory velocity tuning was also observed in DTN units, with most cells exhibiting the deepest inhibitory modulation at 25.6 degrees/s. The majority of LTN and DTN units were driven most effectively through the eye contralateral to the recording site. Nonetheless, a large percentage of LTN (78%) and DTN (93%) cells could be driven to some extent through both eyes. Despite this conspicuous ipsilateral eye influence, no units were found in either the LTN or the DTN that were driven solely through the ipsilateral eye.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neural activity in dorsolateral pontine nucleus of alert monkey during ocular following responses.

1. Movements of the visual scene evoke short-latency ocular following responses. To study the neural mediation of the ocular following responses, we investigated neurons in the dorsolateral pontine nucleus (DLPN) of behaving monkeys. The neurons discharged during brief, sudden movements of a large-field visual stimulus, eliciting ocular following. Most of them (100/112) responded to movements of a large-field visual stimulus with directional selectivity. 2. Response amplitude was measured in two components of the neural response: an initial transient component and a late sustained component. Most direction-selective DLPN neurons showed their strongest responses at high stimulus speeds (80-160 degrees/s), whether their response components were initial (63/87, 72%) or sustained (63/87, 72%). The average firing rates of 87 DLPN neurons increased as a linear function of the logarithm of stimulus speed up to 40 degrees/s for both initial and sustained responses. 3. Not only the magnitude but also the latency of the neural and ocular responses were dependent on stimulus speed. The latencies of both neural and ocular responses were inversely related to the stimulus speed. As a result, the time difference between the response latencies for neural and ocular responses did not vary much with changes of stimulus speed. 4. Response latency was measured when a large-field random dot pattern was moved in the preferred direction and at the preferred speed of each neuron. Seventy-three percent (56/77) of the neurons were activated less than 50 ms after the onset of the stimulus motion. In most cases (67/77, 87%), their increase of firing rate started before the eye movements, and 34% of them (26/77) started greater than 10 ms before the eye movements. 5. Blurring of the random dot pattern by interposing a sheet of ground glass increased the latency of both neural responses and eye movements. On the other hand, the blurred images did not change the timing of the effect of blanking the visual scene on the responses of the neurons or eye movements. 6. When a check pattern was used instead of random dots, both neural and ocular responses began to decrease rapidly when the temporal frequency of the visual stimulus exceeded 20 Hz. When the temporal frequency of the visual stimulus approached 40 Hz, the neurons showed a distinctive burst-and-pause firing pattern. The eye movements recorded at the same time showed signs of oscillation, and their temporal patterns were closely correlated to those of the firing rate.(ABSTRACT TRUNCATED AT 400 WORDS)     

Direction and speed tuning to visual motion in cortical areas MT and MSTd during smooth pursuit eye movements

When tracking a moving target in the natural world with pursuit eye movement, our visual system must compensate for the self-induced retinal slip of the visual features in the background to enable us to perceive their actual motion. We previously reported that the speed of the background stimulus in space is represented by dorsal medial superior temporal (MSTd) neurons in the monkey cortex, which compensate for retinal image motion resulting from eye movements when the direction of the pursuit and background motion are parallel to the preferred direction of each neuron. To further characterize the compensation observed in the MSTd responses to the background motion, we recorded single unit activities in cortical areas middle temporal (MT) and MSTd, and we selected neurons responsive to a large-field visual stimulus. We studied their responses to the large-field stimulus in the background while monkeys pursued a moving target and while fixated a stationary target. We investigated whether compensation for retinal image motion of the background depended on the speed of pursuit. We also asked whether the directional selectivity of each neuron in relation to the external world remained the same even during pursuit and whether compensation for retinal image motion occurred irrespective of the direction of the pursuit. We found that the majority of the MSTd neurons responded to the visual motion in space by compensating for the image motion on the retina resulting from the pursuit regardless of pursuit speed and direction, whereas most of the MT neurons responded in relation to the genuine retinal image motion.     

Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation

1. Pursuit eye movements are usually made against a visual background that is moved across the retina by the pursuit movement. We have investigated the effect of this visual stimulation on the response of pursuit cells that lie within the superior temporal sulcus (STS) of the monkey. 2. We assigned these pursuit cells to one of two groups depending on the nature of their preferred visual stimulus. One group of cells, comprising all cells located in the dorsal-medial region of the medial superior temporal area (MSTd) and some cells in lateral-anterior MST (MST1), responded to the motion of a large patterned field but showed little or no response to small spots or slits. The other group, consisting of all foveal middle temporal area (MTf) cells and many MST1 cells, responded preferentially to small spot motion or equally well to small spot motion or large field. 3. For many pursuit cells that preferred large-field stimuli, the visual response showed a reversal of the preferred direction of motion as the size of the stimulus field increased. The reversal usually occurred as the size of the moving random-dot field used as a stimulus increased in size from 20 x 20 degrees to 30 x 30 degrees for motion at approximately 10 degrees/s. The size of the filed stimulus leading to reversal of preferred direction depended on the speed of stimulus motion. Higher speeds of motion required larger stimulus fields to produce a reversal of preferred direction. This reversal (of preferred direction) did not reflect a center-surround organization of the receptive field but seemed to reflect the spatial summation properties of these cells. 4. For three-quarters of the cells that preferred large-field stimulation, the preferred direction of motion for the large field was opposite to the preferred direction of the pursuit response. The remaining cells showed either the same preferred directions for large-field visual stimulation and the pursuit response or had bidirectional visual responses. If we consider only the cells that show a reversal of preferred direction for large- and small-field stimuli, the preferred direction for the large field was always the opposite to that of pursuit, and the preferred direction for the small field was always the same. 5. During pursuit against a lighted background, the cells that showed opposite preferred directions for large-field stimulation and pursuit had synergistic responses--a facilitation of the pursuit response over the response during pursuit in the dark. Slow pursuit speeds (less than 20 degrees/s) produced the greatest facilitation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Initiation of smooth-pursuit eye movements to first-order and second-order motion stimuli

Since normal human subjects can perform smooth-pursuit eye movements only in the presence of a moving target, the occurrence of these eye movements represents an ideal behavioural probe to monitor the successful processing of visual motion. It has been shown previously that subjects can execute smooth-pursuit eye movements to targets defined by luminance and colour, the first-order stimulus attributes, as well as to targets defined by derived, second-order stimulus attributes such as contrast, flicker or motion. In contrast to these earlier experiments focusing on steady-state pursuit, the present study addressed the course of pre-saccadic pursuit initiation (less than 100 ms), as this early time period is thought to represent open-loop pursuit, i.e. the eye movements are exclusively driven by visual inputs proceeding the onset of the eye movement itself. Eye movements of five human subjects tracking first- and second-order motion stimuli had been measured. The analysis of the obtained eye traces revealed that smooth-pursuit eye movements could be initiated to first-order as well as second-order motion stimuli, even before the execution of the first initial saccade. In contrast to steady-state pursuit, the initiation of pursuit was not exclusively determined by the movement of the target, but rather due to an interaction between dominant first-order and less-weighted second-order motion components. Based on our results, two conclusions may be drawn: first and specific for initiation of smooth-pursuit eye movements, we present evidence supporting the notion that initiation of pursuit reflects integration of all available visual motion information. Second and more general, our results further support the hypothesis that the visual system consists of more than one mechanism for the extraction of first-order and second-order motion.     

Prediction and a stationary, structured visual background influence the dynamics of the smooth-pursuit offset in humans

 It is still not clear whether the transition from pursuit eye movements to fixation is mediated by the same system that initiates pursuit, or whether another system, a specialized fixation system, is responsible. To investigate this question we measured smooth-pursuit eye movements and smooth-pursuit termination in five normal subjects using both predictable and unpredictable step-ramp stimuli (velocities 10° and 20°/s) in front of a homogeneous and a structured visual background in order to compare the profile of eye velocity under these different conditions. With the predictable and/or structured visual background there was a gradual transition of eye velocity toward zero. In contrast, with the unpredictable stimulus in front of a homogeneous background, eye velocity during the offset was characterized by an overshoot (on the average, 2.2±1.0°/s for 10°/s ramps) before eye velocity settled at zero. Under this condition, steady-state velocity gain and the deceleration of the offset were significantly higher than during the other paradigm with the same target velocity. The latency of the pursuit offset was significantly shorter when a predictable stimulus was used. The duration of the offset did not depend on the experimental condition used. These findings imply that the pursuit onset and offset have some similarities and may be mediated by the same oculomotor system. Received: 6 February 1998 / Accepted: 8 July 1998     

Smooth-pursuit eye movements elicited by first-order and second-order motion

 The perception of the displacement of luminance-defined contours (i.e., first-order motion) is an important and well-examined function of the visual system. It can be explained, for example, by the operation of elementary motion detectors (EMDs), which cross-correlate the spatiotemporal luminance distribution. More recent studies using second-order motion stimuli, i.e., shifts of the distribution of features such as contrast, texture, flicker, or motion, extended classic concepts of motion perception by including nonlinear or hierarchical processing in the EMD. Smooth-pursuit eye movements can be used as a direct behavioral probe for motion processing. The ability of the visual system to extract motion signals from the spatiotemporal changes of the retinal image can be addressed by analyzing the elicited eye movements. We measured the eye movement response to moving objects defined by two different types of first-order motion and two different types of second-order motion. Our results clearly showed that the direction of smooth-pursuit eye movements was always determined by the direction of object motion. In particular, in the case of second-order motion stimuli, smooth-pursuit did not follow the retinal image motion. The latency of the initial saccades during pursuit of second-order stimuli was slightly but significantly increased, compared with the latency of saccades elicited by first-order motion. The processing of second-order motion in the peripheral visual field was less exact than the processing of first-order motion in the peripheral field. Steady state smooth-pursuit eye speed did not reflect the velocity of second-order motion as precisely as that of first-order motion, and the resulting retinal error was compensated by saccades. Interestingly, for slow second-order stimuli we observed that the eye could move faster than the target, leading to small, corrective saccades in the opposite direction to the ongoing smooth-pursuit eye movement. We conclude from our results that both visual perception and the control of smooth-pursuit eye movements have access to processing mechanisms extracting first- and second-order motion. Received: 26 August 1996 / Accepted: 8 November 1996     

The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity

1. Purkinje cell activity was recorded from lobules VI and VII of the cerebellar vermis during the performance of visuooculomotor tasks designed to dissociate the signals related to head, smooth-pursuit eye, and retinal image movements. Task-related modulations in the simple spike discharge rates of 157 cells were observed in three alert monkeys. 2. Of 65 Purkinje cells that were completely tested for all three signals, all exhibited smooth-pursuit eye movement-related activity. An additional vestibular or visual response was observed in 17 and 11% of the cells, respectively. Eye, head, and retinal image velocity signals were all recorded in the same unit in 52% of the Purkinje cells. The responses of 5% of the fully tested cells were associated with changes in the direction of eye, head, and retinal image movement. 3. The observed sensorioculomotor responses were direction selective in 98% of the Purkinje cells. For the Purkinje cells that were fully tested, 60% of the cells exhibited peak discharge rates for ipsilateral and 40% for contralateral eye velocity. Of these Purkinje cells, 45% exhibited eye, head, and retinal image velocity signals with equivalent direction preferences. 4. Of 42 Purkinje cells tested, 88% demonstrated some kinds of interactive responses during combined eye and sensory stimulation. The interaction of eye and head velocity signals has been discussed in a companion paper (38). The modulation in discharge rate observed during tracking in the presence of a random dot background pattern could be predicted from the dissociated responses to smooth pursuit in the dark and to movements of the background pattern during suppression of eye movements. 5. The sensitivity to smooth-pursuit eye velocity averaged 1.4 times the sensitivity to head velocity. In 80% of the Purkinje cells, however, the sensitivity to eye velocity exceeded the sensitivity to head velocity by an average of only 10%. The sensitivity to smooth-pursuit eye velocity averaged 1.6 times the sensitivity to retinal image velocity. 6. An increase in Purkinje cell discharge rate was observed during the open-loop period of the initiation of smooth-pursuit eye movements. This open-loop response was consistent with the presence of a visual signal during ocular pursuit, since these cells were also shown to be responsive to a dissociated retinal image velocity signal. Furthermore, the magnitude of the open-loop response indicated an enhancement of the sensitivity to retinal image velocity when visual information became behaviorally significant.(ABSTRACT TRUNCATED AT 400 WORDS)     

Primate area MST-l is involved in the generation of goal-directed eye and hand movements

The contributions of the middle superior temporal area (MST) in the posterior parietal cortex of rhesus monkeys to the generation of smooth-pursuit eye movements as well as the contributions to motion perception are well established. Here, we present the first experimental evidence that this area also contributes to the generation of goal-directed hand movements toward a moving target. This evidence is based on the outcome of intracortical microstimulation experiments and transient lesions by small injections of muscimol at identified sites within the lateral part of area MST (MST-l). When microstimulation was applied during the execution of smooth-pursuit eye movements, postsaccadic eye velocity in the direction of the preferred direction of the stimulated site increased significantly (in 93 of 136 sites tested). When microstimulation was applied during a hand movement trial, the hand movement was displaced significantly in the same direction (in 28 of 39 sites tested). When we lesioned area MST-l transiently by injections of muscimol, steady-state eye velocity was exclusively reduced for ipsiversive smooth-pursuit eye movements. In contrast, hand movements were displaced toward the contralateral side, irrespective of the direction of the moving target. Our results provide evidence that area MST-l is involved in the processing of moving targets and plays a role in the execution of smooth-pursuit eye movements as well as visually guided hand movements.     

The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

 We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information. Received: 17 June 1996 / Accepted: 29 April 1997     

Neural correlates of reafference: evoked brain activity during motion perception and saccadic eye movements

The ability to perceive a stable visual environment despite eye movements and the resulting displacement of the retinal image is a striking feature of visual perception. In order to study the brain mechanism related to this phenomenon, an EEG was recorded from 30 electrodes spaced over the occipital, temporal and parietal brain areas while stationary or moving visual stimuli with velocities between 178 degrees/s and 533 degrees/s were presented. The visual stimuli were presented both during saccadic eye movements and with stationary eyes. Stimulus-related potentials were measured, and the effects of absolute and relative stimulus velocity were analyzed. Healthy adults participated in the experiments. In all 36 subjects and experimental conditions, four potential components were found with mean latencies of about 70, 140, 220 and 380 ms. The latency of the two largest components between 100 and 240 ms decreased while field strength increased with higher absolute stimulus velocity for both stationary and moving eyes, whereas relative stimulus velocity had no effect on amplitude, latency and topography of the visual evoked potential (VEP) components. If the visual system uses retinal motion information only, we would expect a dependence upon relative velocity. Since field strength and latency of the components were independent of eye movements but dependent upon absolute stimulus velocity, the visual cortex must use extraretinal information to extract stimulus velocity. This was confirmed by the fact that significant topographic changes were observed when brain activity evoked during saccades and with stationary eyes was compared. In agreement with the reafference principle, the findings indicate that the same absolute visual stimulus activates different neuronal elements during saccades than during fixation.     

Human smooth pursuit: stimulus-dependent responses

We studied pursuit eye movements in seven normal human subjects with the scleral search-coil technique. The initial eye movements in response to unpredictable changes in target motion were analyzed to determine the effect of target velocity and position on the latency and acceleration of the response. By restricting our analysis to the presaccadic portion of the response we were able to eliminate any saccadic interactions, and the randomized stimulus presentation minimized anticipatory responses. This approach has allowed us to characterize a part of the smooth-pursuit system that is dependent primarily on retinal image properties. The latency of the smooth-pursuit response was very consistent, with a mean of 100 +/- 5 ms to targets moving 5 degrees/s or faster. The responses were the same whether the velocity step was presented when the target was initially stationary or after tracking was established. The latency did increase for lower velocity targets; this increase was well described by a latency model requiring a minimum target movement of 0.028 degrees, in addition to a fixed processing time of 98 ms. The presaccadic accelerations were fairly low, and increased with target velocity until an acceleration of about 50 degrees/s2 was reached for target velocities of 10 degrees/s. Higher velocities produced only a slight increase in eye acceleration. When the target motion was adjusted so that the retinal image slip occurred at increasing distances from the fovea, the accelerations declined until no presaccadic response was measurable when the image slip started 15 degrees from the fovea. The smooth-pursuit response to a step of target position was a brief acceleration; this response occurred even when an oppositely directed velocity stimulus was present. The latency of the pursuit response to such a step was also approximately 100 ms. This result seems consistent with the idea that sensory pathways act as a low-pass spatiotemporal filter of the retinal input, effectively converting position steps into briefly moving stimuli. There was a large asymmetry in the responses to position steps: the accelerations were much greater when the position step of the target was away from the direction of tracking, compared with steps in the direction of tracking. The asymmetry may be due to the addition of a fixed slowing of the eyes whenever the target image disappears from the foveal region. When saccades were delayed by step-ramp stimuli, eye accelerations increased markedly approximately 200 ms after stimulus onset.(ABSTRACT TRUNCATED AT 400 WORDS)     

Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI-VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR x1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR x1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.     

Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation

Extracellular recordings were obtained from 319 input units and 304 Purkinje cells (P-cells) in the dorsal paraflocculus of alert monkeys trained to fixate a visual target. They changed discharge rates with either eye movement, eye position, or visual stimulus movement. Of the 319 input units, recorded in the granular layer or white matter, most were mossy fibers (MFs), but 90 (28%) showed characteristic cellular spikes. The latter units were probably granular cells (p-GC). Of the 319 input units, 163 (51%) showed bursts with saccades (burst units) and 62 (19%) showed a prelude on the average 124 ms prior to the onset of saccade (long-lead burst units). Sixty-five (20%) had tonic activity related to eye position and also showed bursts with saccades (burst-tonic units), and the remaining 29 (9%) showed only tonic activity (tonic units). MFs and p-GCs showed no significant differences in the proportion of each type of unit or in their response properties. The majority of burst units (63%) were pan directional, whereas all long-lead burst units had directional selectivity. The preferred directions of long-lead burst, burst tonic, and directionally selective burst units were found in all four quadrants. Position-related activity was found in 48% of the burst-tonic and tonic units to be linearly related to eye position and to show position threshold. The other units also had position thresholds but their activity was not monotonically related to fixation position. Six climbing fibers (CFs), 32 input units (including 13 p-GC), and 8 P-cells showed cyclic responses during sinusoidal movements of a visual pattern. One class of MF units (57%) responded only to the direction, whereas the others responded to both the direction and retinal-slip velocity. Both CF and P-cell units responded to sinusoidal retinal-slip velocity. Of 67 input units, 23 showed cyclic modulation in firing during sinusoidal eye movements in the horizontal plane. Nineteen were burst-tonic and four were tonic units. They also showed position sensitivity. The phase of the cyclic responses tended to lag behind the eye velocity during low-frequency trackings. Of 237 P-cells, 163 (68.8%) discharged with saccades (burst P-cells), 42 (17.7%) paused with saccades (pause P-cells), and 32 (13.5%) discharged with saccades in one direction and paused in the other (burst-pause P-cells). Position sensitivity was found in 38 P-cells; 12 were burst, 5 were pause, and 10 were burst-pause P-cells. Eleven did not respond with saccades.(ABSTRACT TRUNCATED AT 400 WORDS)     

Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

The smooth-pursuit system moves the eyes in space accurately to track slowly moving objects of interest despite visual inputs from the moving background and/or vestibular inputs during head movements. Recently, our laboratory has shown that young primates exhibit asymmetric eye movements during vertical pursuit across a textured background; upward eye velocity gain is reduced. To further understand the nature of this asymmetry, we performed three series of experiments in young monkeys. In Experiment 1, we examined whether this asymmetry was due to an un-compensated downward optokinetic reflex induced by the textured background as it moves across the retina in the opposite direction of the pursuit eye movements. For this, we examined the monkeys’ ability to fixate a stationary spot in space during movement of the textured background and compared it with vertical pursuit across the stationary textured background. We also examined gains of optokinetic eye movements induced by downward motion of the textured background during upward pursuit. In both task conditions, gains of downward eye velocity induced by the textured background were too small to explain reduced upward eye velocity gains. In Experiment 2, we examined whether the frame of reference for low-velocity, upward pursuit was orbital or earth vertical. To test this, we first applied static tilt in the roll plane until the animals were nearly positioned on their side in order to dissociate vertical or horizontal eye movements in the orbit from those in space. Deficits were observed for upward pursuit in the orbit but not in space. In Experiment 3, we tested whether asymmetry was observed during head-free pursuit that requires coordination between eye and head movements. Asymmetry in vertical eye velocity gains was still observed during head-free pursuit although it was not observed in vertical head velocity. These results, taken together, suggest that the asymmetric eye movements during vertical pursuit are specific for upward, primarily eye pursuit in the orbit.