Blink-perturbed saccades in monkey. II. Superior colliculus activity

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency ( approximately 10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10-30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.     

Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. I. Suppression of ipsilateral saccades

When a saccade occurs to an interesting object, visual fixation holds its image on the fovea and suppresses saccades to other objects. Electrical stimulation of the frontal eye field (FEF) has been reported to elicit saccades, and recently also to suppress saccades. This study was performed to characterize properties of the suppression of visually guided (Vsacs) and memory-guided saccades (Msacs) induced by electrical stimulation of the FEF in trained monkeys. For any given stimulation site, we determined the threshold for electrically evoked saccades (Esacs) at < or =50 microA and then examined suppressive effects of stimulation at the same site on Vsacs and Msacs. FEF stimulation suppressed the initiation of both Vsacs and Msacs during and about 50 ms after stimulation at stimulus intensities lower than those for eliciting Esacs, but did not affect the vector of these saccades. Suppression occurred for ipsiversive but not contraversive saccades, and more strongly for saccades with larger amplitudes and those with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for suppression was about 50 ms before saccade onset, which suggests that suppression occurred in the efferent pathway for generating Vsacs at the premotor rather than the motoneuronal level, most probably in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of ipsilateral saccades were distributed over the classical FEF where saccade-related movement neurons were observed. The results suggest that the FEF may play roles in not only generating contraversive saccades but also maintaining visual fixation by suppressing ipsiversive saccades.     

Velocity prediction in corrective saccades during smooth-pursuit eye movements in monkey

Summary It has been noted in a variety of studies in both humans and monkeys that saccades made during smooth pursuit eye movements are usually quite accurate. Since saccades are known to be planned on the basis of neuronal information existing at some interval of time before the actual onset of the movement, it is generally accepted that some sort of prediction or use of visual motion velocity is combined with static position error in the execution of these saccades to moving targets. However, statistical treatment of this response in humans has provided evidence for alternative mechanisms, including a strategy of saccading ahead in the direction of target motion without any incorporation of actual speed information about target motion in the response. We reinvestigated this question quantitatively in the monkey on a large data base of saccades. We found evidence that supports the hypothesis that information about target speed per se is used in this species in the production of saccades to moving targets. Multiple linear regression analysis supported the hypothesis that information about the position error and the target velocity that exists at about 100 ms prior to the saccade onset are both required to provide a statistical explanation of saccade size during pursuit eye movements under the conditions of our experiments.     

Behavioral properties of saccades generated as a choice response

The behavior characterizing choice response decision-making was studied in monkeys to provide background information for ongoing neurophysiological studies of the neural mechanisms underlying saccadic choice decisions. Animals were trained to associate a specific color from a set of colored visual stimuli with a specific spatial location. The visual stimuli (colored disks) appeared briefly at equal eccentricity from a central fixation position and then were masked by gray disks. The correct target association was subsequently cued by the appearance of a colored stimulus at the fixation point. The animal indicated its choice by saccading to the remembered location of the eccentric stimulus, which had matched the color of the cue. The number of alternative associations (NA) varied from 1 to 4 and remained fixed within a block of trials. After the training period, performance (percent correct responses) declined modestly as NA increased (on average 96, 93 or 84% correct for 1, 2 or 4 NA, respectively). Response latency increased logarithmically as a function of NA, thus obeying Hick’s law. The spatial extent of the learned association between color and location was investigated by rotating the array of colored stimuli that had remained fixed during the learning phase to various different angles. Error rates in choice saccades increased gradually as a function of the amount of rotation. The learned association biased the direction of the saccadic response toward the quadrant associated with the cue, but saccade direction was always toward one of the actual visual stimuli. This suggests that the learned associations between stimuli and responses were not spatially exact, but instead the association between color and location was distributed with declining strength from the trained locations. These results demonstrate that the saccade system in monkeys also displays the characteristic dependence on NA in choice response latencies, while more basic features of the eye movements are invariant from those in other tasks. The findings also provide behavioral evidence that spatially distributed regions are established for the sensory-to-motor associations during training which are later utilized for choice decisions.     

Representation of averaging saccades in the superior colliculus of the monkey

We tested the hypothesis that averaging saccades occur when two different saccades are prepared and executed simultaneously. The activity of saccade-related burst neurons (SRBNs) in the primate superior colliculus was recorded while monkeys made both non-averaging saccades to single targets and averaging saccades which directed the gaze between two simultaneously presented visual targets. For movements of comparable direction and amplitude, the activity measured during averaging and non-averaging saccades was statistically indistinguishable. These results are not consistent with the hypothesis that averaging saccades result from the simultaneous execution of two different saccades at the level of the collicular SRBNs. Instead, these findings indicate that averaging saccades are represented as single intermediate movements within the topographically organized map of these collicular cells.     

Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. II. Suppression of bilateral saccades

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and approximately 50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was approximately 40-50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at < or =40 microA but usually did not evoke any saccades at 80 microA and were different from those of ipsilateral saccades where stimulation evoked saccades at < or =50 microA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.     

Unit activity related to spontaneous saccades in frontal dorsomedial cortex of monkey

Summary Single unit activity was studied in the dorsomedial edge of the frontal lobe, above the superior arcuate sulcus in three trained monkeys (Macaca nemestrina). Gaze and head movements were recorded with two magnetic search coils. Discharges preceding spontaneous eye movements in a preferred direction were consistently observed in light and in dark, in a limited cortical territory at the anterior border of the supplementary motor area. Microstimulation at these sites elicited saccades in the unit preferred direction. Five presaccadic units were studied head fixed and head free and showed the same saccade-related activity under both conditions. Preliminary data suggest that the area studied may be a supplementary eye field distinct from the arcuate frontal eye field.     

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)     

Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades.

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys' performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.     

Dynamic properties of eye position coded neurons in the alert monkey during saccades

Summary Single units in the regions of the III, IV and VI nuclei were recorded together with EOG's for horizontal and vertical eye positions in alert macaques. The sequential analysis of several dynamic parameters of the activity patterns in correlation to the saccade velocity for saccades in the on-direction leads to the results that: 1. eye position coded neurons can clearly be separated into two main classes [early peak (EP) and late peak (LP)] by means of their activity patterns during saccades in the on-direction; 2. the maximum impulse rate of EP neurons shows a better correlation with saccade velocity than the difference between maximum and initial impulse rate while the opposite is valid for LP neurons. EP neurons are likely to be motoneurons which initiate saccadic eye movements whereas LP neurons are too slow for this task because they reach their maximum impulse rate after half the saccadic time. The dynamic properties of LP neurons have several features similar to those of primary stretch receptors during ramp-like stretches. The possible influence of fusimotor activity on the oculomotor system is discussed. The fact that the relationship between dynamic index and saccade velocity shows subgroups of data supports the assumption that the state of alertness changes instantaneously in untrained monkeys.Supported in part by the National Eye Institute, U.S. Public Health Service under grant EY-00592 to Dr. G. Westheimer and by the Deutsche Forschungsgemeinschaft.     

Context dependent amplitude modulations of express and regular saccades in man and monkey

Saccadic reaction times and amplitudes were determined in four human subjects and two rhesus monkeys when they made saccades to visual targets appearing in different spatial or temporal contexts. Two stimuli were presented at different positions, either simultaneously (global condition) or in random order (range condition). Both the gap and the overlap paradigm were used. The characteristics of different groups of saccades defined by the separate peaks in the distribution of the saccadic reaction times as express and regular saccades, were analysed and compared. It is shown that, in man and monkey, the amplitudes of express saccades undergo the same or even stronger context-dependent changes as do those of regular saccades. Furthermore, the presence or absence of the fixation point also influences the saccadic amplitudes, at least for the express saccades. We conclude that the neural mechanisms that determine the amplitudes of the express saccades are more strictly under the control of the physical and physiological conditions of the stimulus situation, whereas regular saccades have greater — although not complete — dependence on the psychological context and, in particular, the subject's effort.     

Auditory saccades from different eye positions in the monkey: implications for coordinate transformations

Auditory spatial information arises in a head-centered coordinate frame, whereas the saccade command signals generated by the superior colliculus (SC) are thought to specify target locations in an eye-centered frame. However, auditory activity in the SC appears to be neither head- nor eye-centered but in a reference frame that is intermediate between both of these reference frames. This neurophysiological finding suggests that auditory saccades might not fully compensate for changes in initial eye position. Here, we investigated whether the accuracy of saccades to sounds is affected by initial eye position in rhesus monkeys. We found that, on average, a 12 degrees horizontal shift in initial eye position produced only a 0.6 to 1.6 degrees horizontal shift in the endpoints of auditory saccades made to targets at a range of locations along the horizontal meridian. This shift was similar in size to the modest influence of eye position on visual saccades. This virtually complete compensation for initial eye position implies that auditory activity in the SC is read out in a manner that is appropriate for generating accurate saccades to sounds.     

Fourier analysis of saccades in monkeys and humans

1. By recording eye movements with the search coil technique and subjecting them to an accurate infinite Fourier transform algorithm, we describe the Fourier spectra of human and monkey saccades. In both species we find heretofore undescribed features consisting of a regular pattern of local minima in the power plot, which cannot be attributed to noise. The frequency of these minima is well correlated with saccade duration. 2. Computer simulation shows that if the pulse component of the saccade is considered to be rectangular, then the first of these minima (called M1) occurs at a frequency that is the reciprocal of the duration of the pulse. 3. Comparing the position of this component during individual monkey saccades with electrophysiological recordings of motoneurons during the same saccades leads to the conclusion that these minima are related to the burst components in ocular motoneuron discharges. Specifically, the reciprocals of the frequencies of these minima are correlated with the duration of the burst component in the motoneuron discharge. 4. In the Fourier spectra of human saccades, the relationship of the frequency of M1 to saccadic duration is a function similar to that in the monkey. This adds to the evidence that the human saccade also is driven by a pulse-step signal. 5. In both monkeys and humans, T1, the reciprocal of the frequency of M1, is shorter than both the saccade duration and the burst duration of individual motoneurons, even though neurophysiological studies in monkeys generally report the saccadic burst duration to be equal to the saccade duration. This probably arises because the saccadic pulse is not rectangular, with the extremes contributing very little energy to the Fourier spectrum. By further computer modeling we show these shape effects explicitly: as the rise- and falltime increase, making the pulse less rectangular, T1 becomes shorter; in addition, as the asymmetry of rise and fall increases, the depth of the minima is reduced. We conclude that T1 measures the "effective pulse" duration of the motoneuron. 6. There is a difference in the relationship of effective pulse duration to the saccade duration between short and long saccades. For saccades shorter than approximately 40 ms in the human and 50 ms in the monkey, the pulse width as measured by this technique varies little with saccade duration. For longer saccades, effective pulse width increases linearly with duration. We agree with others that for short saccades the pulse is both height- and width-modulated; but for longer saccades, height modulation saturates and only width modulation remains.(ABSTRACT TRUNCATED AT 400 WORDS)     

Firing behaviour of squirrel monkey eye movement-related vestibular nucleus neurons during gaze saccades

The firing behaviour of vestibular nucleus neurons putatively involved in producing the vestibulo-ocular reflex (VOR) was studied during active and passive head movements in squirrel monkeys. Single unit recordings were obtained from 14 position-vestibular (PV) neurons, 30 position-vestibular-pause (PVP) neurons and 9 eye-head-vestibular (EHV) neurons. Neurons were sub-classified as type I or II based on whether they were excited or inhibited during ipsilateral head rotation. Different classes of cell exhibited distinctive responses during active head movements produced during and after gaze saccades. Type I PV cells were nearly as sensitive to active head movements as they were to passive head movements during saccades. Type II PV neurons were insensitive to active head movements both during and after gaze saccades. PVP and EHV neurons were insensitive to active head movements during saccadic gaze shifts, and exhibited asymmetric sensitivity to active head movements following the gaze shift. PVP neurons were less sensitive to ondirection head movements during the VOR after gaze saccades, while EHV neurons exhibited an enhanced sensitivity to head movements in their on direction. Vestibular signals related to the passive head movement were faithfully encoded by vestibular nucleus neurons. We conclude that central VOR pathway neurons are differentially sensitive to active and passive head movements both during and after gaze saccades due primarily to an input related to head movement motor commands. The convergence of motor and sensory reafferent inputs on VOR pathways provides a mechanism for separate control of eye and head movements during and after saccadic gaze shifts.     

Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey

Summary In the alert monkey we have compared the properties of saccades elicited by a visual stimulus (V-saccades) with those generated by electrical stimulation in the superior colliculus (E-saccades). We found that whereas there exists a graded relation betweenE-saccade amplitude and current strength,E-saccade direction is remarkably independent of electrical stimulation parameters. At sufficiently high current strengths (about 20 A),E-saccades are consistently directed toward the center of the movement field of nearby cells, except when stimulation is performed at sites near the collicular borders. Further interesting differences between the amplitude and direction behaviour were observed when the variability inE-saccade vectors, obtained with fixed stimulation parameters, was analyzed. In all cases,E-saccade amplitude scatter exceeds direction scatter, suggesting the possibility of a polar coordinate organization for the coding of saccade metrics. These data are compared withV-saccade scatter data, recently obtained in the human (Van Opstal and Van Gisbergen 1989 c). Finally, an analysis of saccade dynamics shows thatE-saccades can reachV-saccadic velocities at higher current strengths. However, at near-threshold current strengths, whereE-saccade amplitude decreases (see above), we found at most stimulation sites (22/37) thatE-saccades are consistently slower thanV-saccades of the same amplitude. Possible mechanisms underlying the collicular role in saccade generation are discussed.