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.     

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.     

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     

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.     

Saccadic and smooth pursuit eye movements: computational modeling of a common inhibitory mechanism in brainstem

The oculomotor system coordinates different types of eye movements in order to orient the visual axis, including saccade and smooth pursuit,. It was traditionally thought that the premotor pathways for these different eye movements are largely separate. In particular, a group of midline cells in the pons called omnipause neurons were considered to be part of only the saccadic system. Recent experimental findings have shown activity modulation of these brainstem premotor neurons during both kinds of eye movements. In this study, we propose a new computational model of the brainstem circuitry underlying the generation of saccades and smooth pursuit eye movements. Similar models have been developed earlier, but mainly looking at pure saccades. Here, we integrated recent neurophysiological findings on omnipause neuron activity during smooth pursuit. Our computational model can mimic some new experimental findings as the similarity of "eye velocity profile" with "omnipause neuron pattern of activity" in pursuit movement. We showed that pursuit neuron activity is augmented during catch-up saccades; this increment depends on the initial pursuit velocity in catch-up saccade onset. We conclude that saccadic and pursuit components of catch-up saccades are added to each other nonlinearly.     

Common inhibitory mechanism for saccades and smooth-pursuit eye movements

The premotor pathways subserving saccades and smooth-pursuit eye movements are usually thought to be different. Indeed, saccade and smooth-pursuit eye movements have different dynamics and functions. In particular, a group of midline cells in the pons called omnipause neurons (OPNs) are considered to be part of the saccadic system only. It has been established that OPNs keep premotor neurons for saccades under constant inhibition during fixation periods. Saccades occur only when the activity of OPNs has completely stopped or paused. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The premotor relay for smooth pursuit is thought to be organized differently and omnipause neurons are not supposed to be involved in smooth-pursuit eye movements. To investigate this supposition, OPNs were recorded during saccades and during smooth pursuit in the monkey (Macaca mulatta). Unexpectedly, we found that neuronal activity of OPNs decreased during smooth pursuit. The resulting activity reduction reached statistical significance in approximately 50% of OPNs recorded during pursuit of a target moving at 40 degrees /s. On average, activity was reduced by 34% but never completely stopped or paused. The onset of activity reduction coincided with the onset of smooth pursuit. The duration of activity reduction was correlated with pursuit duration and its intensity was correlated with eye velocity. Activity reduction was observed even in the absence of catch-up saccades that frequently occur during pursuit. Electrical microstimulation in the OPNs' area induced a strong deceleration of the eye during smooth pursuit. These results suggest that OPNs form an inhibitory mechanism that could control the time course of smooth pursuit. This inhibitory mechanism is part of the fixation system and is probably needed to avoid reflexive eye movements toward targets that are not purposefully selected. This study shows that saccades and smooth pursuit, although they are different kinds of eye movements, are controlled by the same inhibitory system.     

Effects of voluntary blinks on saccades,vergence eye movements,and saccade-vergence interactions in humans

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20 degrees up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7 degrees and combined saccade-vergence movements with a version amplitude of 20 degrees. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.     

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.     

Evidence that the superior colliculus participates in the feedback control of saccadic eye movements

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17 degrees. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.     

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)     

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.     

Saccade-related inhibitory input to pontine omnipause neurons: an intracellular study in alert cats.

Omnipause neurons (OPNs) are midline pontine neurons that are thought to control a number of oculomotor behaviors, especially saccades. Intracellular recordings were made from OPNs in alert cats to elucidate saccade-associated postsynaptic events in OPNs and thereby determine what patterns of afferent discharge impinge on OPNs to cause their saccadic inhibition. The membrane potential of impaled OPNs exhibited steep hyperpolarization before each saccade that lasted for the whole period of the saccade. The hyperpolarization was reversed to depolarization by intracellular injection of Cl- ions, indicating it consisted of temporal summation of inhibitory postsynaptic potentials (IPSPs). The duration of the saccade-related hyperpolarization was almost equal to the duration of the concurrent saccades. The time course of the hyperpolarization was similar to that of the radial eye velocity except for the initial phase. During the falling phase of eye velocity, the correlation between the instantaneous amplitude of hyperpolarization and the instantaneous eye velocity was highly significant. The amplitude of hyperpolarization at the eye velocity peak was correlated significantly with the peak eye velocity. The time integral of the hyperpolarization was correlated with the radial amplitude of saccades. The initial phase disparity between the hyperpolarization and eye velocity was due to the relative constancy of peak time (approximately 20 ms) of the initial steep hyperpolarization regardless of the later potential profile that covaried with the eye velocity. The initial steep hyperpolarization led the beginning of saccades by 15.9 +/- 3.8 (SD) ms, which is longer than the lead time for medium-lead burst neurons. These results demonstrate that the pause of activity in OPNs is caused by IPSPs initiated by an abrupt, intense input and maintained, for the whole duration of the saccade, by afferents conveying eye velocity signals. We suggest that the initial sudden inhibition originates from central structures such as the superior colliculus and frontal eye fields and that the eye velocity-related inhibition originates from the burst generator in the brain stem.     

Glycinergic inputs cause the pause of pontine omnipause neurons during saccades

Pontine omnipause neurons (OPNs) are inhibitory neurons projecting to saccade-related premotor burst neurons. OPNs exhibit sustained discharge during fixations and cease firing before and during saccades. The pause in OPN discharge releases the burst neurons from tonic inhibition, resulting in generation of saccadic eye movements. OPNs are thought to receive two major inhibitory inputs during saccades: an early component that determines the pause onset and a late component that controls the pause duration. Although there is evidence that numerous glycinergic and GABAergic terminals contact OPNs, their physiological roles remain unclear. To reveal functions of glycinergic and GABAergic inputs, we investigated effects of iontophoretic application of strychnine, a glycine receptor antagonist, and bicuculline, a GABAA receptor antagonist, on discharge patterns of OPNs in alert cats. Application of strychnine reduced the ratio of pause duration to saccade duration. Analysis of the timing of pause relative to saccades showed that pause onset was delayed and pause end was advanced. These effects were observed for saccades in all directions. Application of bicuculline, in contrast, had no effect on the OPN pause duration or timing. Both strychnine and bicuculline increased tonic firing rate during intersaccadic intervals. These results suggest that glycinergic, but not GABAergic, afferents convey inhibitory signals that determine the onset as well as duration of pause in OPN activity during saccades.     

The effect of microstimulation of the oculomotor vermis on discharges of fastigial neurons and visually-directed saccades in macaques

The present study confirmed our previous reports that neurons in the fastigial oculomotor region (FOR) of the macaque show presaccadic bursts during contralateral saccades and that the burst duration is closely related to the duration of the accompanying saccade. Furthermore, when the burst duration was reduced by subthreshold electrical stimulation applied to the oculomotor vermis prior to the onset of the burst, the impending visually-directed saccade became hypometric. The reduction in the burst duration was closely related to the degree of the hypometria. Since saccadic burst neurons in the FOR constitute the sole output channel for saccadic signals of the oculomotor vermis, the findings support the hypothesis that the cerebellum can regulate the amplitude of eye movements.     

Premotor inhibitory neurons carry signals related to saccade adaptation in the monkey

Cerebellar output changes during motor learning. How these changes cause alterations of motoneuron activity and movement remains an unresolved question for voluntary movements. To answer this question, we examined premotor neurons for saccadic eye movement. Previous studies indicate that cells in the fastigial oculomotor region (FOR) within the cerebellar nuclei on one side exhibit a gradual increase in their saccade-related discharge as the amplitude of ipsiversive saccades adaptively decreases. This change in FOR activity could cause the adaptive change in saccade amplitude because neurons in the FOR project directly to the brain stem region containing premotor burst neurons (BNs). To test this possibility, we recorded the activity of saccade-related burst neurons in the area that houses premotor inhibitory burst neurons (IBNs) and examined their discharge during amplitude-reducing adaptation elicited by intrasaccadic target steps. We specifically analyzed their activity for off-direction (contraversive) saccades, in which the IBN activity would increase to reduce saccade size. Before adaptation, 29 of 42 BNs examined discharged, at least occasionally, for contraversive saccades. As the amplitude of contraversive saccades decreased adaptively, half of BNs with off-direction spike activity showed an increase in the number of spikes (14/29) or an earlier occurrence of spikes (7/14). BNs that were silent during off-direction saccades before adaptation remained silent after adaptation. These results indicate that the changes in the off-direction activity of BNs are closely related to adaptive changes in saccade size and are appropriate to cause these changes.     

Saccade-related neurons in the primate fastigial nucleus: what do they encode?

The cerebellar fastigial oculomotor region (FOR) and the overlying oculomotor vermis (OV) are involved in the control of saccadic eye movements, but nature and function of their saccade-related neuronal signals are not fully understood. There is controversy in at least two major aspects: first, lesion studies in OV/FOR reported eye-position-dependent dysmetria-with FOR lesions, centripetal saccades became more hypermetric than centrifugal saccades-suggesting that the cerebellum may compensate for orbital mechanics. However, single-unit studies failed to reveal corresponding eye-position dependencies in FOR saccade-related discharge patterns. Second, some single-unit studies reported precise correlation between burst and saccade duration in the FOR. However, others stated that FOR bursts were only weakly related to saccade properties. In an attempt to resolve these discrepancies, we recorded single FOR units in monkeys that made horizontal saccades (16 degrees ) from different starting positions. Sampling saccades of one fixed amplitude and application of an objective, computer-based burst-detection-routine allowed us to correlate burst parameters (onset latency, peak latency, peak amplitude, number of spikes, duration) and kinematic properties of individual saccades. FOR bursts were found to start and peak earlier and exhibit higher peak burst amplitudes for faster than for slower saccades of the same amplitude. While these correlations between FOR bursts and saccade properties were statistically significant for a minority of approximately 20-25% of individual units, the same effects were also predominant in the remainder of the neuronal sample and statistically significant on the population level. Neuronal activity was not significantly modulated by eye position itself. However, reflecting differences in saccade velocities but not an actual influence of eye position per se, FOR bursts for centripetal and centrifugal saccades exhibited subtle but systematic differences, which closely paralleled, and hence probably explain, the eye-position dependency of deficits observed after FOR inactivation. Our findings indicate that FOR signals reflect much of the kinematic properties of the saccade. Moreover, they are consistent with the idea that the FOR output is purposefully modified according to these kinematic properties to maintain saccadic accuracy.     

Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey

The interstitial nucleus of Cajal (iC) is known to be the neural integrator for vertical and torsional eye movements. Burst-tonic neurons are thought to be the neural substrate for this function. Until now, the iC has not been specifically considered to play a part in saccade generation. The aim of this study was to characterize saccade-related burst neurons in the iC during torsional and vertical eye movements. Saccade-related burst neurons were recorded in the iC of macaque monkeys during fast phases of torsional and vertical vestibular nystagmus, spontaneous and visually guided eye movements, and in light and darkness. Burst neurons in the iC (n=85) were found intermingled between burst-tonic and tonic neurons. They were not spontaneously active, showed no eye position sensitivity, and responded during saccades and quick phases of nystagmus with a burst of activity whose duration was closely correlated with saccade amplitude and hence saccade duration (correlation coefficients up to 0.9). Latency in the on-direction was, on average, 10.4 ms (range 5–23 ms); it decreased with different saccade directions and became negative in the off-direction. In a horizontal-vertical coordinate system, on-direction of the majority of neurons was either upward (n=52) or downward (n=33). There was no horizontal on-direction. Burst neurons of different vertical on-directions were found intermingled throughout the iC. In the vertical-torsional plane, on-direction always showed an ipsiversive torsional component, i.e., a clockwise (positive) torsion for neurons in the right iC and a counterclockwise (negative) torsional component when recorded in the left iC. The findings indicate that saccade-related burst neurons in the iC control coordinate axes for vertical and torsional quick eye rotations. As in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), burst neurons in the iC encode vertical saccades with an ipsitorsional direction with similar burst characteristics. It is suggested that iC burst neurons play a part in the local feedback loop of the reciprocal iC-riMLF projections.     

Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques.

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the "marginal zone"). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral "on" directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Visual-ocular motor activity in the macaque pregeniculate complex

The anatomical connections of the pregeniculate complex (PrGC) with components of the visual-ocular motor system suggested its contribution to ocular motor behavior. Subsequent studies reported saccade-related activity in the primate PrGC. To determine its contribution, we characterized pregeniculate units (n = 128) in alert macaques during ocular motor tasks and visual stimulation. We found that 36/109 saccade-related units exhibited postsaccadic bursts or pauses in tonic discharge for saccades of any amplitude or direction. In contrast to previous results, 46/109 responses preceded or coincided with the saccade, while 47/109 responses were directionally tuned. Pregeniculate units were modulated not only in association with saccades (109/128) but also with smooth eye movements and visual motion (20/128) or eye position (23/128). Multiple ocular motor signals were recorded from 19% of the units, indicating signal convergence on individual neurons. Visual responses were demonstrated in 51% of PrGC units: visual field illumination modulated the resting discharge of 33 units; the responses of 37 saccade-related units and all 23 position-dependent units were modulated by visual stimulation. Early saccadic activity in the PrGC suggests that it contributes more to gaze than postsaccadic modulation of visual or ocular motor activity. The patterns of saccadic responses and the modulation of PrGC activity in association with a variety of visual-ocular motor behaviors suggest its potential role as a relay between the parietal cortex and elements of the brain stem ocular motor pathways, such as the superior colliculus and pretectal nucleus of the optic tract.     

Oblique saccadic eye movements of primates

The objective of these experiments was to determine whether the trajectories of the horizontal and vertical components of oblique saccades in primates were coupled. Human and monkey eye movements were recorded during a visual tracking task that jumped a small visible target spot to different locations on a tangent screen. For oblique saccades larger than ca. 3 deg, there was coupling between the horizontal and vertical components so that the duration of the smaller component was longer ("stretched") than would have been expected from its amplitude-duration relationship. The duration of a stretched component of an oblique saccade was linearly related to the vector amplitude of the eye movement but not to the amplitude of the stretched component. Stretched components of oblique saccades had lower peak and average velocities than would have occurred with pure horizontal or vertical saccades of the same size. Decreased component velocity was not caused by low-velocity eye movement components inserted at the beginning or end of the saccade, but was a function of the saccade's direction and component amplitude. For any saccade, there was a linear relationship between peak and average component velocity. We compared the discharge of monkey abducens neurons with the characteristics of the on-direction horizontal components of oblique saccades. The burst duration of an abducens neuron was lengthened when the horizontal component of an oblique saccade was stretched. Intraburst firing frequency was also decreased in correspondence with a decrease in horizontal component velocity. For an oblique saccade, the duration of the neuron's burst was correlated with the duration of the horizontal component and with the vector amplitude of the saccade, but was not correlated with the amplitude of the horizontal component itself. The duration of the smaller component of an oblique saccade was proportional but not always equal to the duration of the larger component. Usually, the smaller component began later and ended earlier than the larger component. These results show that the horizontal and vertical components of oblique saccades are coupled centrally so that the velocity of the smaller component is decreased and its duration is increased. For oblique saccades, larger than ca. 3 deg, amplitude-duration and amplitude-velocity relationships based on pure horizontal or vertical saccade data are not applicable. These findings are discussed in relation to three recently proposed models of coupled saccadic burst generators.