Response characteristics of neurons in the pulvinar of awake cats to saccades and to visual stimulation

We studied responses of pulvinar neurons in awake cats that were allowed to execute spontaneous eye movements. Extracellular cell activity during saccades, saccade-like image shifts, and various stationary visual stimuli was recorded together with the animals' eye positions. All neurons analyzed had receptive fields that covered most of the central 80x80 degrees of the animals' visual field and did only respond to large (>20 degrees) visual stimuli. According to their response properties, recorded neurons were divided into three populations. The first group, termed "S neurons" (16%), responded when the animals performed saccades but were unresponsive to any of the visual stimuli tested. These neurons do not seem to receive a visual input that is strong enough to drive them. The second group, termed "V neurons" (51%), responded to various visual stimuli including saccade-like image motion when the eyes were stationary, but not when the animals executed saccades. V neurons therefore distinguish retinal image movements that are generated externally from internally generated image motion. Finally, "SV neurons" (31%) responded when the animals made saccades as well as to saccade-like image motion or to stationary stimuli. Although these neurons do not distinguish self-induced retinal image motion from motion generated by external stimulus movements, they must receive non-retinal motion-related input, because responses elicited by saccades had shorter latencies than responses to saccade-like stimulus movements. Only SV neurons resemble response properties of pretectal neurons that project to the pulvinar and that comprise the major subcortical visual input. The functional significance of pulvinar neuronal populations for visual and visuomotor information processing is discussed.     

Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness

Saccade-related burst neurons were recorded in the caudal part of the fastigial nucleus (fastigial oculomotor region) during spontaneous eye movements and fast phases of optokinetic and vestibular nystagmus in light and darkness from three macaque monkeys. All neurons (n=47) were spontaneously active and exhibited a burst of activity with each saccade and fast phase of nystagmus. Most neurons (n=31) only exhibited a burst of activity, whereas those remaining also exhibited a pause in firing rate before or after the burst. Burst parameters varied considerably for similar saccades. For horizontal saccades all neurons, except for three, had a preferred direction with an earlier onset of burst activity to the contralateral side. For contralateral saccades the burst started on average 17.5 ms before saccade onset, whereas the average lead-time for ipsilateral saccades was only 6.5 ms. Three neurons were classified as isotropic with similar latencies and peak burst activity in all directions. None of the neurons had a preferred direction with an earlier onset of burst activity to the ipsilateral side. Burst duration increased with saccade amplitude, whereas peak burst activity was not correlated with amplitude. There was no relationship between peak burst activity and peak eye velocity. In the dark, neurons generally continued to burst with each saccade and fast phase of nystagmus. Burst for saccades in the dark was compared with burst for saccades of similar amplitude and direction in the light. Saccades in the dark had a longer duration and peak burst activity was reduced on average to 62% (range 36–105%). In three neurons a burst in the dark was no longer clearly distinguishable above the ongoing spontaneous activity. These data suggest that the saccade-related burst neurons in the FOR modify saccadic profiles by directly influencing acceleration and deceleration, respectively, of individual eye movements. This could be achieved by an input to the inhibitory and excitatory burst neurons of the saccadic burst generator in the brainstem. From neuroanatomical studies it is known that FOR neurons project directly to the brainstem regions containing the immediate premotor structures for saccade generation.     

Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus

There is significant controversy regarding the ability of the primate visual system to construct stable percepts from a never-ending stream of brief fixations and rapid saccadic eye movements. In this study, we examined the timing and occurrence of perisaccadic modulation of LGN single-unit activity in awake-behaving macaque monkeys while they made spontaneous saccades in the dark and made visually guided saccades to discrete stimuli located outside the receptive field. Our hypothesis was that the activity of LGN cells is modulated by efference copies of motor plans to produce saccadic eye movements and that this modulation depends neither on the presence of feedforward visual information nor on a corollary discharge of signals directing saccadic eye movements. On average, 25% of LGN cells demonstrated significant perisaccadic modulation. This modulation consisted of a moderate suppression of activity that began more than 100 ms prior to the initiation of a saccadic eye movement and continued beyond the termination of the saccadic eye movement. This suppression was followed by a large enhancement of activity after the eyes arrived at the next fixation. Although members of all three LGN relay cell classes (magnocellular, parvocellular, and koniocellular) demonstrated significant saccade-related suppression and enhancement of activity, more cells demonstrated postsaccadic enhancement (25%) than perisaccadic suppression (17%). In no case did the timing of the modulation coincide directly with saccade duration. The degree of modulation observed did not vary with LGN cell class, LGN receptive field center location, center sign (ON-center or OFF-center), or saccade latency or velocity. The time course of modulation did, however, vary with saccade size such that suppression was longer for longer saccades. The fact that activity from a percentage of LGN cells from all cell classes was modulated in relationship to saccadic eye movements in the absence of direct visual stimulation suggests that this modulation is a general phenomenon not tied to specific types of visual stimuli. Similarly, because the onset of the modulation preceded eye movements by more than 100 ms, it is likely that this modulation reflects higher order motor-planning rather than a corollary of mechanisms in direct control of eye movements themselves. Finally, the fact that the largest modulation is a postsaccadic enhancement of activity may suggest that perisaccadic modulations are designed more for the facilitation of visual information processing once the eyes land at a new location than for filtering unwanted visual stimuli.     

Dynamic coding of vertical facilitated vergence by premotor saccadic burst neurons

To redirect our gaze in three-dimensional space we frequently combine saccades and vergence. These eye movements, known as disconjugate saccades, are characterized by eyes rotating by different amounts, with markedly different dynamics, and occur whenever gaze is shifted between near and far objects. How the brain ensures the precise control of binocular positioning remains controversial. It has been proposed that the traditionally assumed "conjugate" saccadic premotor pathway does not encode conjugate commands but rather encodes monocular commands for the right or left eye during saccades. Here, we directly test this proposal by recording from the premotor neurons of the horizontal saccade generator during a dissociation task that required a vergence but no horizontal conjugate saccadic command. Specifically, saccadic burst neurons (SBNs) in the paramedian pontine reticular formation were recorded while rhesus monkeys made vertical saccades made between near and far targets. During this task, we first show that peak vergence velocities were enhanced to saccade-like speeds (e.g., >150 vs. <100 degrees/s during saccade-free movements for comparable changes in vergence angle). We then quantified the discharge dynamics of SBNs during these movements and found that the majority of the neurons preferentially encode the velocity of the ipsilateral eye. Notably, a given neuron typically encoded the movement of the same eye during horizontal saccades that were made in depth. Taken together, our findings demonstrate that the brain stem saccadic burst generator encodes integrated conjugate and vergence commands, thus providing strong evidence for the proposal that the classic saccadic premotor pathway controls gaze in three-dimensional space.     

A quantitative analysis of the correlations between eye movements and neural activity in the pretectum

The study of the saccadic system has focused mainly on neurons active before the beginning of saccades, in order to determine their contribution in movement planning and execution. However, most oculomotor structures contain also neurons whose activity starts only after the onset of saccades, the maximum of their activity sometimes occurring near saccade end. Their characteristics are still largely unknown. We investigated pretectal neurons with saccade-related activity in the alert cat during eye movements towards a moving target. They emitted a high-frequency burst of action potentials after the onset of saccades, irrespective of their direction, and will be referred to as "pretectal saccade-related neurons". The delay between saccade onset and cell activity varied from 17 to 66 ms on average. We found that burst parameters were correlated with the parameters of saccades; the peak eye velocity was correlated with the peak of the spike density function, the saccade amplitude with the number of spikes in the burst, and burst duration increased with saccade duration. The activity of six pretectal saccade-related neurons was studied during smooth pursuit at different velocities. A correlation was found between smooth pursuit velocity and mean firing rate. A minority of these neurons (2/6) were also visually responsive. Their visual activity was proportional to the difference between eye and target velocity during smooth pursuit (retinal slip). These results indicate that the activity of pretectal saccade-related neurons is correlated with the characteristics of eye movements. This finding is in agreement with the known anatomical projections from premotor regions of the saccadic system to the pretectum.     

Saccade-related Purkinje cell activity in the oculomotor vermis during spontaneous eye movements in light and darkness

Saccade-related Purkinje cells (PCs) were recorded in the oculomotor vermis (lobules VI, VII) during spontaneous eye movements and fast phases of optokinetic and vestibular nystagmus in the light and darkness, from two macaque monkeys. All neurons (n=46) were spontaneously active and exhibited a saccade-related change of activity with all saccades and fast phases of nystagmus. Four types of neurons were found: most neurons (n=31) exhibited a saccade-related burst of activity only (VBN); other units (n=7) showed a burst of activity with a subsequent pause (VBPN); some of the units (n=5) paused in relation to the saccadic eye movement (pause units,VPN); a few PCs (n=3) showed a burst of activity in one direction and a pause of activity in the opposite direction. For all neurons, burst activity varied considerably for similar saccades. There were no activity differences between spontaneous saccades and vestibular or optokinetically elicited fast phases of nystagmus. The activity before, during, and after horizontal saccades was quantitatively analyzed. For 24 burst PCs (VBN, VBPN), the burst started before saccade onset in one horizontal direction (preferred direction), on average by 15.3 ms (range 27-5 ms). For all these neurons, burst activity started later in the opposite (non-preferred) direction, on average 4.9 ms (range 20 to -12 ms, P<0.01) before saccade onset. The preferred direction could be either with ipsilateral (42% of neurons) or contralateral (58%) saccades. Nine burst PCs had similar latencies and burst patterns in both horizontal directions. The onset of burst activity of a minority of PCs (n=5) lagged saccade onset in all directions. The pause for VBPN neurons started after the end of the saccade and reached a minimum of activity some 40–50 ms after saccade completion. For all saccades and quick phases of nystagmus, burst duration increased with saccade duration. Peak burst activity was not correlated with saccade amplitude or peak eye velocity. PCs continued to show saccade-related burst activity in the dark. However, in 59% of the PCs (VBN, VBPN), peak burst activity was significantly reduced in the dark (on average 28%, range 15–36%) when saccades with the same amplitude (but longer duration in the dark) were compared. For VBP neurons, the pause component after the saccade disappeared in the dark. The difference in peak burst activity (light vs darkness) is similar to that seen for saccade-related neurons in the fastigial oculomotor region (FOR, the structure receiving direct input from vermal PCs) and suggests that the oculomotor vermis also might affect saccade acceleration and/or deceleration. The findings indicate that in the oculomotor vermis — in contrast to the FOR — several different types of saccade-related neurons (PCs) are found. However, the vast majority of PCs behave qualitatively similar to FOR neurons with regard to the burst activity pattern and a direction-specific burst activity onset starting well before saccade onset. This latency will allow these neurons to influence the initiation of saccades in the saccadic brainstem generator through multisynaptic pathways. At present, it has to be determined how (saccade-related) PC activity determines FOR activity.     

Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF)

The integrity of the paramedian pontine reticular formation (PPRF) is necessary for the generation of rapid eye movements. The main saccade-related population is of the burst type with latencies between 0 and 40 ms preceding a saccade, and they can be divided into medium- and long-lead burst neurons. Burst neurons have predominantly spatially coded movement fields in the rostral PPRF, while in the caudal PPRF they increase their burst strength in temporal coding approximately in the pulling directions of extraocular eye muscles (i.e. almost horizontal or vertical). Both neuronal populations have ipsilateral on-directions and contain long-lead burst neurons. In a quantitative analysis the firing patterns of long-lead burst neurons are compared to those of medium-lead burst neurons, which form the predominant output of the saccadic pulse generator to the motoneurons. The firing patterns of temporally coded long-lead bursters are similar to those of medium-lead bursters, except for earlier on-latencies, larger statistical fluctuations, and specializations for small or large saccades in oblique directions. The spatially coded burst neurons form a motor map of saccadic vectors. The diameter of their movement field is often about the size of the saccade vector, and they encode saccadic onset and duration. These results are consistent with a model for visual saccades in eye displacement coordinates, where the spatio-temporal recording of horizontal eye movements is effected by long-lead burst neurons in the PPRF.     

The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)     

Activity of mesencephalic vertical burst neurons during saccades and smooth pursuit

The activity of vertical burst neurons (BNs) was recorded in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF-BNs) and in the interstitial nucleus of Cajal (NIC-BNs) in head-restrained cats while performing saccades or smooth pursuit. BNs emitted a high-frequency burst of action potentials before and during vertical saccades. On average, these bursts led saccade onset by 14 +/- 4 ms (mean +/- SD, n = 23), and this value was in the range of latencies ( approximately 5-15 ms) of medium-lead burst neurons (MLBNs). All NIC-BNs (n = 15) had a downward preferred direction, whereas riMLF-BNs showed either a downward (n = 3) or an upward (n = 5) preferred direction. We found significant correlations between saccade and burst parameters in all BNs: vertical amplitude was correlated with the number of spikes, maximum vertical velocity with maximum of the spike density, and saccade duration with burst duration. A correlation was also found between instantaneous vertical velocity and neuronal activity during saccades. During fixation, all riMLF-BNs and approximately 50% of NIC-BNs (7/15) were silent. Among NIC-BNs active during fixation (8/15), only two cells had an activity correlated with the eye position in the orbit. During smooth pursuit, most riMLF-BNs were silent (7/8), but all NIC-BNs showed an activity that was significantly correlated with the eye velocity. This activity was unaltered during temporary disappearance of the visual target, demonstrating that it was not visual in origin. For a given neuron, its ON-direction during smooth pursuit and saccades remained identical. The activity of NIC-BNs during both saccades and smooth pursuit can be described by a nonlinear exponential function using the velocity of the eye as independent variable. We suggest that riMLF-BNs, which were not active during smooth pursuit, are vertical MLBNs responsible for the generation of vertical saccades. Because NIC-BNs discharged during both saccades and pursuit, they cannot be regarded as MLBNs as usually defined. NIC-BNs could, however, be the site of convergence of both the saccadic and smooth pursuit signals at the premotoneuronal level. Alternatively, NIC-BNs could participate in the integration of eye velocity to eye position signals and represent input neurons to a common integrator.     

Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey

The cortical area V6A, located in the dorsal part of the anterior bank of the parieto-occipital sulcus, contains retino- and craniocentric visual neurones together with neurones sensitive to gaze direction and/or saccadic eye movements, somatosensory stimulation and arm movements. The aim of this work was to study the dynamic characteristics of V6A saccade-related activity. Extracellular recordings were carried out in six macaque monkeys performing a visually guided saccade task with the head restrained. The task was performed in the dark, in both the dark and light, and sometimes in the light only. The discharge of certain neurones during saccades is due to their responsiveness to visual stimuli. We used a statistical method to distinguish responses due to visual stimulation from those responsible for saccadic control. Out of 597 V6A neurones tested, 66 (11%) showed responses correlated with saccades; 26 of 66 responded also to visual stimulation and 31 of 66 did not; the remaining 9 were not visually tested. We calculated the response latency to saccade onset and its inter-trial variance in 24 of 66 neurones. Saccade neurones could respond before, during or after the saccade. Neurones responding before saccade-onset or during saccades had much higher latency variance than neurones responding after saccades. The early-responding cells had a mean latency (±SD) of –64±62 ms, while the late-responding cells a mean latency of +89±20 ms. The responses to saccadic eye movements were directionally sensitive and varied with the amplitude of the saccade. Responses of late-responding cells disappeared in complete darkness. We suggest that the activity of early-responding cells represents the intended saccadic eye movement or the shift of attention towards another part of the visual space, whereas that of late-responding cells is a visual response due to retinal stimulation during saccades. Electronic Publication     

Evidence against direct connections to PPRF EBNs from SC in the monkey

Direct projections from the superior colliculus (SC) to the paramedian pontine reticular formation (PPRF) have been demonstrated anatomically. The PPRF contains cells called excitatory burst neurons (EBNs) that execute the final premotoneuronal processing for saccadic eye movements, as well as other burst cells called long-lead burst neurons (LLBNs). Previous electrophysiological tests in monkey have failed to find evidence for monosynaptic connections from the SC to EBNs, but have shown that direct projections to LLBNs exist. The validity of these results has been questioned because EBNs are known to be inhibited during periods of fixation by cells called omnipause neurons (OPNs). In later experiments in cat, the stimulus in the SC was triggered during saccades (when OPNs are off) and direct connections to EBNs were found. The present experiments were conducted to determine whether direct connections from the SC to EBNs could be demonstrated in monkey. LLBNs located near EBNs were also recorded. Single-pulse stimuli were delivered at sites in the SC at current levels well above those required to evoke saccades with pulse train stimuli. The stimuli were triggered shortly after the onset of ipsilateral or contralateral saccades and also slightly after the end of saccades. A sample of 21 EBNs was recorded and none were activated by postsaccadic stimulation or during contralateral saccades. The high spontaneous discharge rates of EBNs during ipsilateral saccades made activation of these cells more difficult to detect; however, when the results were quantified by peristimulus time histograms aligned on stimulus onset, only 1/21 EBNs showed evidence of activation in the monosynaptic range of latencies (<1.6 ms), 13 EBNs were activated at di- or polysynaptic latencies, and 7 were not activated. In contrast, 15/21 LLBNs were activated with latencies in the monosynaptic range. Further evidence supporting the absence of direct connections to EBNs was obtained by realigning the peristimulus time histograms for a subset of EBNs with similar firing rates on the time of occurrence of the last spike before stimulus onset. A subset of EBNs was also studied during drowsy ipsilaterally directed eye drifts, during which these cells were firing at low spontaneous rates and OPNs were off. No evidence for direct connections to EBNs was found in this behavioral state. The variance in results obtained for cat and monkey may be due to a species difference that reflects the more complex signal processing required in the monkey's saccadic system.     

Shortening and prolongation of saccade latencies following microsaccades

When the eyes fixate at a point in a visual scene, small saccades rapidly shift the image on the retina. The effect of these microsaccades on the latency of subsequent large-scale saccades may be twofold. First, microsaccades are associated with an enhancement of visual perception. Their occurrence during saccade target perception could, thus, decrease saccade latencies. Second, microsaccades are likely to indicate activity in fixation-related oculomotor neurons. These represent competitors to saccade-related cells in the interplay of gaze holding and shifting. Consequently, an increase in saccade latencies would be expected after microsaccades. Here, we present evidence for both aspects of microsaccadic impact on saccade latency. In a delayed response task, participants made saccades to visible or memorized targets. First, microsaccade occurrence up to 50 ms before target disappearance correlated with 18 ms (or 8%) faster saccades to memorized targets. Second, if microsaccades occurred shortly (i.e., <150 ms) before a saccade was required, mean saccadic reaction time in visual and memory trials was increased by about 40 ms (or 16%). Hence, microsaccades can have opposite consequences for saccade latencies, pointing at a differential role of these fixational eye movements in the preparation of saccade motor programs.     

Sensorimotor integration in the primate superior colliculus. I. Motor convergence

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.     

Discharges of relay cells in lateral geniculate nucleus of the cat during spontaneous eye movements in light and darkness.

1. Discharges of 315 relay cells of the lateral geniculate nucleus (LGN) during spontaneous eye movements were studied in alert cats. 2. When tested in a stationary patterned field, 114 cells showed sustained discharges related to the direction of gaze (S cells) and to local differences in luminance; 109 cells showed transient response to quick shifts of retinal image during saccades (T cells); ninety-two cells showed mixed responses (M cells), i.e. transient responses to rapid shifts of retinal image and sustained firing related to local differences in luminance. 3. Following saccades occurring in the light, T and M cells showed a burst discharge, while spontaneous discharges of S cells were completely suppressed for 150-200 msec. 4. When tested in total darkness, modifications in activity which were apparent in light disappeared completely. This was true for all 315 relay cells. 5. T cells responded to optic chiasm stimulation at shorter latencies (X = 1.15 msec) than S cells (X = 1.77 msec). M cells showed a latency distribution in between those for S and T cells with a mean latency 1.40 msec. 6. When tested with moving grating stimulation, S cells responded in only one manner; with discharges to each stripe of the grating (primary response), while T and M cells showed two different responses: a primary response to a slower motion and a non-specific burst in response to a faster motion. The burst did not reflect the stimulus pattern (secondary response). 7. When tested with diffuse light switched on and off over the tangent screen, S cells showed a sustained response either to light or darkness, whereas T and M cells responded transiently either to the onset or offset of the light, or to both. M cells occasionally showed a mixture of transient and sustained responses either to light or darkness. 8. In over-all response properties, most S cells correspond to X (sustained) cells and most T cells to Y (transient) cells previously known from acute experiments. M cells had intermediate response properties between X and Y cells. 9. Functional roles of these classes of cells in relation to previously proposed functions are discussed.     

Role of the rostral superior colliculus in active visual fixation and execution of express saccades.

1. In the rostral pole of the monkey superior colliculus (SC) a subset of neurons (fixation cells) discharge tonically when a monkey actively fixates a target spot and pause during the execution of saccadic eye movements. 2. To test whether these fixation cells are necessary for the control of visual fixation and saccade suppression, we artificially inhibited them with a local injection of muscimol, an agonist of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). After injection of muscimol into the rostral pole of one SC, the monkey was less able to suppress the initiation of saccades. Many unwanted visually guided saccades were initiated less than 100 ms after onset of a peripheral visual stimulus and therefore fell into the range of express saccades. 3. We propose that fixation cells in the rostral SC form part of a fixation system that facilitates active visual fixation and suppresses the initiation of unwanted saccadic eye movements. Express saccades can only occur when activity in this fixation system is reduced.     

Role of the cat substantia nigra pars reticulata in eye and head movements I. Neural activity

Summary 1. Single unit activity was recorded in the Substantia Nigra pars reticulata (SNpr) of cats trained to orient their gaze toward visual and/or auditory targets. 2. Cells in the SNpr have a steady high rate of spontaneous activity ranging from 35 to 120 spikes per second. The neurons respond to sensory stimuli or in relation to saccadic eye movements with a decrease or a cut-off of the spontaneous discharge. 3. Among 109 cells recorded in the SNPR 60 were responsive to visual stimuli (mean latency = 118 ms). Most of the receptive fields which were plotted were large encompassing part of the ipsilateral field. 4. Thirty nine (39) cells were responsive to auditory stimuli (mean latency = 81 ms). A majority of these cells showed a better response for stimuli located in the contralateral hemifield. 5. In a few cells, the sensory responses were modulated by the subsequent orienting behavior of the animals. 6. Thirty one (31) cells showed a response in relation to saccades. These units typically stopped discharging between 50 and 300 ms prior to the onset of the saccade. 39% of these units also responded in relation to spontaneous saccades in the dark. 61% of the saccadic cells also responded to sensory stimuli in the absence of saccades. Six (6) cells were found to respond to active head movements. 7. These results are discussed in the framework of the role that the basal ganglia might have in the selection of the sensory stimuli that trigger orienting behaviors.     

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)     

Saccade-related Purkinje cells in the cerebellar hemispheres of the monkey

Summary Extracellular single unit discharges of cerebellar Purkinje cells (P-cells) were recorded from the cerebellar hemispheres of two Japanese monkeys (Macaca fuscata) during spontaneous and visually guided eye movements. We found that saccade-related P-cells, whose simple-spike (SS) discharge rates were modulated in close correlation with saccadic eye movements, were localized in fairly restricted areas in the hemisphere, mostly in Crus IIa with some in the deep folia of Crus I. P-cells located in simple lobules, superficial folia of Crus I or in Crus IIp did not change their discharge rate during voluntary eye movements. Fifty-five saccade-related P-cells recorded from Crus I and II showed modulation of SS discharge rate related to both spontaneous and visually triggered saccades, with the modulation closely time-locked to the saccades. Two thirds (37/55) of saccade-related P-cells began to change their SS discharge rate 20–100 ms prior to the onset of saccades. The remaining one third (18/55) changed their activity approximately at the same time as the saccade onset. These saccade-related P-cells did not show changes in activity during smooth pursuit eye movements, and we did not find any P-cells in the cerebellar hemisphere which showed changes of activity preferentially during smooth pursuit eye movements. In about half (26/55) of the saccade-related P-cells, the pattern of modulation prior to and during saccades was biphasic: increase-decrease or decrease-increase. The other half (29/55) showed monophasic increases or decreases. For a given P-cell, the discharge pattern during saccades was similar for saccades of all directions, though there was a preferred direction in the amount of discharge rate modulation. The present findings suggest that the cerebellar hemisphere (Crus I and IIa) plays an important role in the control of voluntary saccadic eye movements, in addition to other cerebellar cortical areas (flocculus and posterior vermis) which are known to participate in the control of saccades.     

The Saccadic system more readily co-processes orthogonal than co-linear saccades

Real-life visual tasks such as tracking jumping objects and scanning visual scenes often require a sequence of saccadic eye movements. The ability of the ocular motor system to parallel process saccades has been previously demonstrated. We recorded the monocular eye movements of five normal human subjects using the magnetic search coil technique in a double step paradigm. Initial target jumps were always purely horizontal or purely vertical. We were interested in the latency to onset of the second saccade as a function of direction in relation to the first saccade. When the inter stimulus interval (ISI) was 150 or 180 ms orthogonal second saccades were of significantly shorter latency than second co-linear saccades. When the ISI was 250 ms the latencies of orthogonal and co-linear second saccades were statistically indistinguishable. Based on these findings it is postulated that the ocular motor system can more readily co-process orthogonal than co-linear saccades.