Parietal representation of object-based saccades

When monkeys make saccadic eye movements to simple visual targets, neurons in the lateral intraparietal area (LIP) display a retinotopic, or eye-centered, coding of the target location. However natural saccadic eye movements are often directed at objects or parts of objects in the visual scene. In this paper we investigate whether LIP represents saccadic eye movements differently when the target is specified as part of a visually displayed object. Monkeys were trained to perform an object-based saccade task that required them to make saccades to previously cued parts of an abstract object after the object reappeared in a new orientation. We recorded single neurons in area LIP of two macaque monkeys and analyzed their activity in the object-based saccade task, as well as two control tasks: a standard memory saccade task and a fixation task with passive object viewing. The majority of LIP neurons that were tuned in the memory saccade task were also tuned in the object-based saccade task. Using a hierarchical generalized linear model analysis, we compared the effects of three different spatial variables on the firing rate: the retinotopic location of the target, the object-fixed location of the target, and the orientation of the object in space. There was no evidence of an explicit object-fixed representation in the activity in LIP during either of the object-based tasks. In other words, no cells had receptive fields that rotated with the object. While some cells showed a modulation of activity due to the location of the target on the object, these variations were small compared to the retinotopic effects. For most cells, firing rates were best accounted for by either the retinotopic direction of the movement, the orientation of the object, or both spatial variables. The preferred direction of these retinotopic and object orientation effects were found to be invariant across tasks. On average, the object orientation effects were consistent with the retinotopic coding of potential target locations on the object. This interpretation is supported by the fact that the magnitude of these two effects were roughly equal in the early portions of the trial, but around the time of the motor response, the retinotopic effects dominated. We conclude that LIP uses the same retinotopic coding of saccade target whether the target is specified as an absolute point in space or as a location on a moving object.     

Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus

Neurons in both the lateral intraparietal area (LIP) of the monkey parietal cortex and the intermediate layers of the superior colliculus (SC) are activated well in advance of the initiation of saccadic eye movements. To determine whether there is a progression in the covert processing for saccades from area LIP to SC, we systematically compared the discharge properties of LIP output neurons identified by antidromic activation with those of SC neurons collected from the same monkeys. First, we compared activity patterns during a delayed saccade task and found that LIP and SC neurons showed an extensive overlap in their responses to visual stimuli and in their sustained activity during the delay period. The saccade activity of LIP neurons was, however, remarkably weaker than that of SC neurons and never occurred without any preceding delay activity. Second, we assessed the dependence of LIP and SC activity on the presence of a visual stimulus by contrasting their activity in delayed saccade trials in which the presentation of the visual stimulus was either sustained (visual trials) or brief (memory trials). Both the delay and the presaccadic activity levels of the LIP neuronal sample significantly depended on the sustained presence of the visual stimulus, whereas those of the SC neuronal sample did not. Third, we examined how the LIP and SC delay activity relates to the future production of a saccade using a delayed GO/NOGO saccade task, in which a change in color of the fixation stimulus instructed the monkey either to make a saccade to a peripheral visual stimulus or to withhold its response and maintain fixation. The average delay activity of both LIP and SC neuronal samples significantly increased by the advance instruction to make a saccade, but LIP neurons were significantly less dependent on the response instruction than SC neurons, and only a minority of LIP neurons was significantly modulated. Thus despite some overlap in their discharge properties, the neurons in the SC intermediate layers showed a greater independence from sustained visual stimulation and a tighter relationship to the production of an impending saccade than the LIP neurons supplying inputs to the SC. Rather than representing the transmission of one processing stage in parietal cortex area LIP to a subsequent processing stage in SC, the differences in neuronal activity that we observed suggest instead a progressive evolution in the neuronal processing for saccades.     

Memory activity of LIP neurons for sequential eye movements simulated with neural networks

Many neurons in macaque lateral intraparietal cortex (LIP) maintain elevated activity induced by visual or auditory targets during tasks in which monkeys are required to withhold one or more planned eye movements. We studied the mechanisms for such memory activity with neural network modeling. Recurrent connections among simulated LIP neurons were used to model memory responses of LIP neurons. The connection weights were computed using an optimization procedure to produce desired outputs in memory-saccade tasks. One constraint for the training process is the "single-purpose" rule, which mimics the fact that once LIP neurons hold the memory activity of a saccade, they are insensitive to further stimuli until the motor action is completed. After training, excitatory connections were developed between units with similar preferred saccade directions, while inhibitory connections were formed between units with dissimilar directions. This "push-pull" mechanism enables the network to encode the next intended eye movement and is essential for programming sequential saccades. In simulating double saccades, the push-pull connections locked the on-going activity in the network for the first saccade until the saccade was made, then a new population of units became active to prepare for the second saccade. The simulated LIP neurons exhibited sensory responses and memory activities similar to those recorded in LIP neurons. We propose that push-pull recurrent connections might be the basic structure mediating the memory activity of area LIP in planning sequential eye movements.     

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 activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a.

1. The cortex of the inferior parietal lobule (IPL) contains neurons whose activity is related to saccadic eye movements. The exact role of the IPL in relation to saccades remains, however, unclear. In this and the companion paper, we approach this problem by quantifying many of the spatial and temporal parameters of the saccade-related (S) activity. These parameters have hitherto been largely unstudied. 2. The activity of single neurons was recorded from Macaca mulatta monkeys while they were performing a delayed-saccade task. The analysis presented here is based on 161 neurons recorded from the lateral intraparietal area (LIP), a recently defined subdivision of the IPL; and 54 neurons recorded from the neighboring part of the IPL, area 7a. Overall, 409 IPL neurons were isolated in this study. 3. The typical activity of IPL neurons during the delayed-saccade task has three basic phases: light sensitive (LS), memory (M), and S. These basic phases are common to neurons of both areas LIP and 7a. In each phase (LS, M, and S), individual neurons may or may not be active. Most LIP neurons, however, are active in more than one phase. 4. To compare the activity levels of different neurons, the actual firing rate was weighted by each neuron's background level, yielding an "activity index" for each neuron, in each phase of the task. We calculated the activity index for the LS and M phases and for three phases related to the saccade: a presaccadic (Pre-S), a saccade-coincident (S-Co), and a postsaccadic (Post-S) phase. For area LIP neurons the median values of the activity index were high for the LS, M, Pre-S, and S-Co activities, and slightly lower in the Post-S period. In area 7a the median values were low for the LS phase and, in particular, for the M and Pre-S phases, somewhat higher coincident with the saccade, and high post-saccadically. 5. In area LIP, in each phase, 49-63% of the neurons had excitatory activity, and 10-17% had inhibitory responses. 6. In contrast, in area 7a excitatory responses were most frequent in the Post-S phase (56%). Excitation was particularly infrequent during M (28%) and Pre-S (22%). The incidence of inhibitory responses varied too (4-18%). The time course of inhibition was roughly opposite that of excitation; the highest frequency of inhibitory responses occurred during the saccade.(ABSTRACT TRUNCATED AT 400 WORDS)     

Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.     

Presaccadic omnidirectional burst activity in the basal interstitial nucleus in the monkey cerebellum

We recorded saccade-related neurons in the vicinity of the dentate nucleus of the cerebellum in two monkeys trained to perform visually guided saccades and memory-guided saccades. Among 76 saccade-related neurons, 38 showed presaccadic bursts in all directions. More than 80% of such burst neurons were located in the area ventral to, not inside, the dentate nucleus, which corresponded to the basal interstitial nucleus (BIN as previously described). We found that the activity of the BIN neurons was correlated with saccade duration but not with saccade amplitude or velocity. Thus, when tested with visually guided saccades, the burst started about 16 ms before saccade onset and ended about 33 ms before saccade offset, regardless of saccade amplitude. The characteristic timing of the BIN cell activity was maintained for different types of saccades (visually guided, memory-guided and spontaneous saccades), which had different dynamics. Although the number of spikes in a burst for each neuron was linearly correlated with saccade amplitude for a given type of saccade, the slope varied depending on the type of saccade. Peak burst frequency was uncorrelated with saccadic peak velocity. In contrast, burst duration was highly correlated with saccade duration regardless of the type of saccade. These results suggest that BIN neurons may carry information to determine the timing of saccades. Received: 14 August 1997 / Accepted: 17 February 1998     

Nonspatial saccade-specific activation in area LIP of monkey parietal cortex

We present evidence that neurons in the lateral intraparietal area (LIP) of monkey posterior parietal cortex (PPC) are activated by the instruction to make an eye movement, even in the complete absence of a spatial target. This study employed a visually guided motor task that dissociated the type of movement to make (saccade or reach) from the location where the movement was to be made. Using this task, animals were instructed to prepare a specific type of movement prior to knowing the spatial location of the movement target. We found that 25% of the LIP neurons recorded in two animals were activated significantly more by the instruction to prepare a saccade than by the instruction to prepare a reach. This finding indicates that LIP is involved in more than merely spatial attention and provides further evidence for nonspatial effector-specific signal processing in the dorsal stream.     

Inactivation of macaque lateral intraparietal area delays initiation of the second saccade predominantly from contralesional eye positions in a double-saccade task

Previous studies have shown that, although lateral intraparietal (LIP) area neurons have retinotopic receptive fields, the response strength of these cells is modulated by eye position. This combining of retinal and eye position information can form a distributed coding of target locations in a head-centered coordinate frame. Such an implicit head-centered coding offers one mechanism for maintaining spatial stability across eye movements and can be used to compute new oculomotor error vectors after each eye movement. An alternative mechanism is to use eye displacement signals rather than eye position signals to maintain spatial stability. The aim of this study was to distinguish which of these two extra-retinal signals (or perhaps both signals) are employed in a double saccade task, which required the monkey to use extraretinal information associated with the first saccade to localize a remembered target for a second saccade. By varying the direction and the end point of the first saccade and selectively inactivating area LIP in one hemisphere with muscimol injection, we were able to distinguish between the two mechanisms by observing how the second saccade was impaired in this task. The displacement mechanism predicts that, if the first saccade is in the contralesional direction, the second saccade will be impaired, and the end point of the first saccade would not be important. The eye position mechanism predicts that if the first saccade ended in the contralesional head-centered space, the second saccade will be impaired, no matter in which direction the first saccade is made. Results showed that, after area LIP lesion, when the first saccade stepped into the contralesional field, the error rate of the second saccade became higher and the latency longer. However, when the end point of the first saccade was constant, the direction of the first saccade had much less effect on the second saccade. These results suggest that eye position, and not eye displacement, is the more predominant factor in this task. In a different behavioral paradigm, the monkeys performed single visual and memory saccades from different initial eye positions. It was found that the impairment of either the metrics or dynamics of visual and memory saccades did not significantly vary with the different eye positions. It thus appears that the performance of single visual and memory saccades is best described in an oculocentric coordinate frame that does not rely on extraretinal signals. Altogether these results lend further support to the hypothesis that, by combining retinal and eye position signals, area LIP contains concurrent eye-centered and head-centered representations of the visual space. Depending on the task, either representation can be used.     

Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys

1. The discharge of 255 neurons in the fastigial nuclei of three trained macaque monkeys was investigated during visually guided saccades. Responses of these neurons were examined also during horizontal head rotation and during microstimulation of the oculomotor vermis (lobules VIc and VII). 2. One hundred and two units were characterized by bursts of firing in response to visually guided saccades. Ninety-eight of these (96.1%) were located within the anatomic confines of the fastigial oculomotor region (FOR), on the basis of reconstruction of recording sites. During contralateral saccades, these neurons showed bursts that preceded the onset of saccades (presaccadic burst), whereas, during ipsilateral saccades, they showed bursts associated with the end of saccades (late saccadic burst). They were hence named saccadic burst neurons. Sixty-one saccadic burst neurons (62.2%) were inhibited during microstimulation of the oculomotor vermis with currents less than 10 microA. 3. All saccadic burst neurons were spontaneously active, and the resting firing rate varied considerably among units, ranging from 10 to 50 imp/s. The tonic levels of activity did not correlate significantly with eye position. 4. The presaccadic burst started 18.5 +/- 4.7 (SD) ms (n = 45) before the onset of saccades in the optimal direction (the direction associated with the maximum values of burst lead time, number of spikes per burst, and burst duration). Optimal directions covered the entire contralateral hemifield, although there was a slightly higher incidence in both horizontal and upper-oblique directions in the present sample. The duration of the presaccadic burst was highly correlated with the duration of saccade (0.85 less than or equal to r less than or equal to 0.97). 5. The late saccadic burst was most robust in the direction opposite to the optimal in each unit (the nonoptimal direction). Its onset preceded the completion of ipsilateral saccade by 30.4 +/- 5.9 ms. The lead time to the end of saccade was consistent among different units and was constant also for saccades of various sizes. Thus the late saccadic burst started even before the saccade onset when the saccade duration was less than 30 ms. Unlike the presaccadic burst, its duration was not related to the duration of saccade. 6. Discharge rates of saccadic burst neurons were correlated neither to eye positions during fixation nor to the initial eye positions before saccades. 7. Eye-position units and horizontal head-velocity units were located rostral to the FOR.(ABSTRACT TRUNCATED AT 400 WORDS)     

Microstimulation of macaque area LIP affects decision-making in a motion discrimination task

A central goal of cognitive neuroscience is to elucidate the neural mechanisms underlying decision-making. Recent physiological studies suggest that neurons in association areas may be involved in this process. To test this, we measured the effects of electrical microstimulation in the lateral intraparietal area (LIP) while monkeys performed a reaction-time motion discrimination task with a saccadic response. In each experiment, we identified a cluster of LIP cells with overlapping response fields (RFs) and sustained activity during memory-guided saccades. Microstimulation of this cluster caused an increase in the proportion of choices toward the RF of the stimulated neurons. Choices toward the stimulated RF were faster with microstimulation, while choices in the opposite direction were slower. Microstimulation never directly evoked saccades, nor did it change reaction times in a simple saccade task. These results demonstrate that the discharge of LIP neurons is causally related to decision formation in the discrimination task.     

Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation.

The lateral intraparietal area (LIP), a region of posterior parietal cortex, was once thought to be unresponsive to auditory stimulation. However, recent reports have indicated that neurons in area LIP respond to auditory stimuli during an auditory-saccade task. To what extent are auditory responses in area LIP dependent on the performance of an auditory-saccade task? To address this question, recordings were made from 160 LIP neurons in two monkeys while the animals performed auditory and visual memory-saccade and fixation tasks. Responses to auditory stimuli were significantly stronger during the memory-saccade task than during the fixation task, whereas responses to visual stimuli were not. Moreover, neurons responsive to auditory stimuli tended also to be visually responsive and to exhibit delay or saccade activity in the memory-saccade task. These results indicate that, in general, auditory responses in area LIP are modulated by behavioral context, are associated with visual responses, and are predictive of delay or saccade activity. Responses to auditory stimuli in area LIP may therefore be best interpreted as supramodal responses, and similar in nature to the delay activity, rather than as modality-specific sensory responses. The apparent link between auditory activity and oculomotor behavior suggests that the behavioral modulation of responses to auditory stimuli in area LIP reflects the selection of auditory stimuli as targets for eye movements.     

Ocular fixation and visual activity in the monkey lateral intraparietal area

The macaque lateral intraparietal area (LIP) has been implicated in visuospatial attention and saccade planning. Since area LIP also contains a representation of the central visual field, we investigated its possible role in fixation and foveal attention in a visual fixation task with gap (momentary disappearance of fixation point). In addition to the expected visual neurons ( n=119), two main categories were identified: (1) cells responding tonically both during the presence and momentary absence of the fixation stimulus( n=47); a subset of these neurons studied in a saccade task showed perisaccadic inhibition in half of the cases (14/27). The timing of this inhibition, however, is only loosely related to saccade timing; (2) cells responding mainly to the absence of the fixation stimulus, with either abrupt or gradual onset of activity during the gap ( n=62). During saccades, these neurons showed presaccadic buildup and/or postsaccadic activity, which was spatially tuned in about half of the tested cells (28/53). Ninety-one percent of the cells in the first category and 59% of the cells in the second category were located in the dorsal portion of area LIP (LIPd). These results are consistent with the hypothesis of an oculomotor-attentional network contributing to fixation engagement and disengagement in a subregion of LIP.     

Saccades and multisaccadic gaze shifts are gated by different pontine omnipause neurons in head-fixed cats

 Pontine omnipause neurons (OPNs) have so far been considered as forming a homogeneous group of neurons whose tonic firing stops during the duration of saccades, when the head is immobilized. In cats, they pause for the total duration of gaze shifts, when the head is free to move. In the present study, carried out on alert cats with fixed heads, we present observations made during self-initiated saccades and during tracking of a moving target which show that the OPN population is not homogeneous. Of the 76 OPNs we identified, 39 were found to have characteristics similar to those of previously described neurons, ”saccade” (S-) OPNs: (1) the durations of their pauses were significantly correlated with the durations of saccades; (2) the discharge ceased shortly before saccade onset and resumed before saccade end; (3) visual responses to target motion were excitatory; and (4) during tracking, S-OPNs interrupted the discharge for the duration of saccades and resumed firing during perisaccadic ”drifts”. However, the characteristics of 37 neurons (”complex” (C-) OPNs) were different: (1) the pause duration was not correlated with the duration of self-initiated saccades; (2) time lead of pause onsets relative to saccades was, on average, longer than in the group of S-OPNs, and firing resumed after the saccade end; (3) visual target motion suppressed tonic discharges; and (4) during tracking, firing was interrupted for the total duration of gaze shifts, including not only saccades but also perisaccadic ”drifts”. We conclude that cat OPNs can be subdivided into two main groups. The first comprises neurons whose firing patterns are compatible with gating individual saccades (”saccade” OPNs). The second group consists of ”complex” OPNs whose firing characteristics are appropriate to gate total gaze displacements rather than individual saccades. The function of these neurons may be to disinhibit pontobulbar circuits participating in the generation of saccade sequences and associated perisaccadic drifts. Received: 20 January 1998 / Accepted: 22 October 1998     

Persistent LIP activity in memory antisaccades: working memory for a sensorimotor transformation

The lateral intraparietal area (LIP) contains neurons that are active during the memory interval of memory saccades. We call these "persistent neurons." Here we study the activity of the persistent neurons in memory antisaccades, "motor" (the saccade is made toward the response field, although the response field is not stimulated visually) and "visual" (the response field is stimulated visually, but the movement is away from the field). Most persistent neurons are active during parts of the memory intervals of both visual and motor memory-antisaccades. Typically, these parts significantly overlap each other and together span the entire memory interval. The amplitude of the activity changes systematically during the memory intervals of visual and motor memory antisaccades. These changes are reflected in an antisaccade differential activity, which turns first to the visual direction and then crosses over to the motor direction. Some persistent neurons appear to show the paradoxical activity previously characterized in visual neurons; paradoxical activity accelerates the transition of the neuron's activity from visual to motor. These observations suggest that the persistent neurons reflect working memory for the computation of the antisaccade sensorimotor transformation. Ensembles of persistent neurons with different response fields may make up modules of working memory.     

Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task.

The close relationship between saccadic eye movements and vision complicates the identification of neural responses associated with each function. Visual and saccade-related responses are especially closely intertwined in a subdivision of posterior parietal cortex, the lateral parietal area (LIP). We analyzed LIP neurons using an antisaccade task in which monkeys made saccades away from a salient visual cue. The vast majority of neurons reliably signaled the location of the visual cue. In contrast, most neurons had only weak, if any, saccade-related activity independent of visual stimulation. Thus, whereas the great majority of LIP neurons reliably encoded cue location, only a small minority encoded the direction of the upcoming saccade.     

Direction selectivity of neurons in the macaque lateral intraparietal area

The lateral intraparietal area (LIP) of the macaque is believed to play a role in the allocation of attention and the plan to make saccadic eye movements. Many studies have shown that LIP neurons generally encode the static spatial location demarked by the receptive field (RF). LIP neurons might also provide information about the features of visual stimuli within the RF. For example, LIP receives input from cortical areas in the dorsal visual pathway that contain many direction-selective neurons. Here we examine direction selectivity of LIP neurons. Animals were only required to fixate while motion stimuli appeared in the RF. To avoid spatial confounds, the motion stimuli were patches of randomly arrayed dots that moved with 100% coherence in eight different directions. We found that the majority (61%) of LIP neurons were direction selective. The direction tuning was fairly broad, with a median direction-tuning bandwidth of 136 degrees. The average strength of direction selectivity was weaker in LIP than that of other areas of the dorsal visual stream but that difference may be because of the fact that LIP neurons showed a tonic offset in firing whenever a visual stimulus was in the RF, independent of direction. Direction-selective neurons do not seem to constitute a functionally distinct subdivision within LIP, because those neurons had robust, sustained delay-period activity during a memory delayed saccade task. The direction selectivity could also not be explained by asymmetries in the spatial RF, in the hypothetical case that the animals attended to slightly different locations depending on the direction of motion in the RF. Our results show that direction selectivity is a distinct attribute of LIP neurons in addition to spatial encoding.     

Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task

Several lines of evidence suggest that the pars reticulata subdivision of the substantia nigra (SNr) plays a role in the generation of saccadic eye movements. However, the responses of SNr neurons during saccades have not been examined with the same level of quantitative detail as the responses of neurons in other key saccadic areas. For this report, we examined the firing rates of 72 SNr neurons while awake-behaving primates correctly performed an average of 136 trials of a visually guided delayed saccade task. On each trial, the location of the visual target was chosen randomly from a grid spanning 40 degrees of horizontal and vertical visual angle. We measured the firing rates of each neuron during five intervals on every trial: a baseline interval, a fixation interval, a visual interval, a movement interval, and a reward interval. We found four distinct classes of SNr neurons. Two classes of neurons had firing rates that decreased during delayed saccade trials. The firing rates of discrete pausers decreased after the onset of a contralateral target and/or before the onset of a saccade that would align gaze with that target. The firing rates of universal pausers decreased after fixation on all trials and remained below baseline until the delivery of reinforcement. We also found two classes of SNr neurons with firing rates that increased during delayed saccade trials. The firing rates of bursters increased after the onset of a contralateral target and/or before the onset of a saccade aligning gaze with that target. The firing rates of pause-bursters increased after the onset of a contralateral target but decreased after the illumination of an ipsilateral target. Our quantification of the response profiles of SNr neurons yielded three novel findings. First, we found that some SNr neurons generate saccade-related increases in activity. Second, we found that, for nearly all SNr neurons, the relationship between firing rate and horizontal and vertical saccade amplitude could be well described by a planar surface within the range of movements we sampled. Finally we found that for most SNr neurons, saccade-related modulations in activity were highly variable on a trial-by-trial basis.     

Primate frontal eye fields. I. Single neurons discharging before saccades

We studied the activity of single neurons in the frontal eye fields of awake macaque monkeys trained to perform several oculomotor tasks. Fifty-four percent of neurons discharged before visually guided saccades. Three different types of presaccadic activity were observed: visual, movement, and anticipatory. Visual activity occurred in response to visual stimuli whether or not the monkey made saccades. Movement activity preceded purposive saccades, even those made without visual targets. Anticipatory activity preceded even the cue to make a saccade if the monkey could reliably predict what saccade he had to make. These three different activities were found in different presaccadic cells in different proportions. Forty percent of presaccadic cells had visual activity (visual cells) but no movement activity. For about half of the visual cells the response was enhanced if the monkey made saccades to the receptive-field stimulus, but there was no discharge before similar saccades made without visual targets. Twenty percent of presaccadic neurons discharged as briskly before purposive saccades made without a visual target as they did before visually guided saccades, and had weak or absent visual responses. These cells were defined as movement cells. Movement cells discharged much less or not at all before saccades made spontaneously without a task requirement or an overt visual target. The remaining presaccadic neurons (40%) had both visual and movement activity (visuomovement cells). They discharged most briskly before visually guided eye movements, but also discharged before purposive eye movements made in darkness and responded to visual stimuli in the absence of saccades. There was a continuum of visuomovement cells, from cells in which visual activity predominated to cells in which movement activity predominated. This continuum suggests that although visual cells are quite distinct from movement cells, the division of cell types into three classes may be only a heuristic means of describing the processing flow from visual input to eye-movement output. Twenty percent of visuomovement and movement cells, but fewer than 2% of visual cells, had anticipatory activity. Only one cell had anticipatory activity as its sole response. When the saccade was delayed relative to the target onset, visual cells responded to the target appearance, movement cells discharged before the saccade, and visuomovement cells discharged in different ways during the delay, usually with some discharge following the target and an increase in rate immediately before the saccade. Presaccadic neurons of all types were actively suppressed following a saccade into their response fields.(ABSTRACT TRUNCATED AT 400 WORDS)     

Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence

It has long been believed that the superior colliculus (SC) is involved in the production of saccades but plays no role in the generation of vergence eye movements. However, results from several recent studies suggest that it may be worthwhile to examine the role of the SC in saccade-vergence interactions. Specifically, the available literature suggests two questions: do saccade-related neurons in SC have three-dimensional movement fields and is the slowing of saccades by vergence attributable, in part, to changes in the level of activity in SC? Single-unit data were recorded from 51 saccade-related neurons in rhesus monkey SC during saccades without vergence, saccades accompanied by convergence, and saccades accompanied by divergence. Most cells (78% for convergence, 86% for divergence) showed a significant reduction in peak spike density when the saccade was accompanied by vergence. A minority of cells (16% for convergence, 2% for divergence) increased their firing rate for saccades accompanied by vergence. Three cells were found that discharged in association with saccades, vergence, and the combination of the two. There were no cells that exhibited the pattern of discharge that would be expected of a cell tuned for saccades with divergence. Thus the present results do not support the hypothesis that saccade-related SC neurons are, as a rule, tuned in three dimensions. Small, but significant, differences in firing rate were often found for saccades without vergence at near and far distances. Approximately half of the cells showed a significant relationship between spike activity and saccade velocity, but the correlations tended to be very weak. This suggests that the decreased neuronal activity of SC neurons has only a limited effect on saccade velocity. For some cells, the movement field shifted for saccades with vergence. These shifts were highly variable from one cell to another.