Saccade-related Burst Neurons Research Articles

The control of eye movements by the cerebellar nuclei: polysynaptic projections from the fastigial, interpositus posterior and dentate nuclei to lateral rectus motoneurons in primates.

Premotor circuits driving extraocular motoneurons and downstream motor outputs of cerebellar nuclei are well known. However, there is, as yet, no unequivocal account of cerebellar output pathways controlling eye movements in primates. Using retrograde transneuronal transfer of rabies virus from the lateral rectus (LR) eye muscle, we studied polysynaptic pathways to LR motoneurons in primates. Injections were placed either into the central or distal muscle portion, to identify innervation differences of LR motoneurons supplying singly innervated (SIFs) or multiply innervated muscle fibers (MIFs). We found that SIF motoneurons receive major cerebellar 'output channels' bilaterally, while oligosynaptic cerebellar innervation of MIF motoneurons is negligible and/or more indirect. Inputs originate from the fastigial nuclei di- and trisynaptically, and from a circumscribed rostral portion of the ventrolateral interpositus posterior and from the caudal pole of the dentate nuclei trisynaptically. While disynaptic cerebellar inputs to LR motoneurons stem exclusively from the caudal fastigial region involved in saccades, pursuit and convergence (via its projections to brainstem oculomotor populations), minor trisynaptic inputs from the rostral fastigial nucleus, which contributes to gaze shifts, may reflect access to vestibular and reticular eye-head control pathways. Trisynaptic inputs to LR motoneurons from the rostral ventrolateral interpositus posterior, involved in divergence (far-response), is likely mediated by projections to the supraoculomotor area, contributing to LR motoneuron activation during divergence. Trisynaptic inputs to LR motoneurons from the caudal dentate, which also innervates disynaptically the frontal and parietal eye fields, can be explained by its superior colliculus projections, and likely target saccade-related burst neurons.

Contribution of the frontal eye field to gaze shifts in the head-unrestrained rhesus monkey: Neuronal activity

The frontal eye field (FEF) has a strong influence on saccadic eye movements with the head restrained. With the head unrestrained, eye saccades combine with head movements to produce large gaze shifts, and microstimulation of the FEF evokes both eye and head movements. To test whether the dorsomedial FEF provides commands for the entire gaze shift or its separate eye and head components, we recorded extracellular single-unit activity in monkeys trained to make large head-unrestrained gaze shifts. We recorded 80 units active during gaze shifts, and closely examined 26 of these that discharged a burst of action potentials that preceded horizontal gaze movements. These units were movement or visuomovement related and most exhibited open movement fields with respect to amplitude. To reveal the relations of burst parameters to gaze, eye, and/or head movement metrics, we used behavioral dissociations of gaze, eye, and head movements and linear regression analyses. The burst number of spikes (NOS) was strongly correlated with movement amplitude and burst temporal parameters were strongly correlated with movement temporal metrics for eight gaze-related burst neurons and five saccade-related burst neurons. For the remaining 13 neurons, the NOS was strongly correlated with the head movement amplitude, but burst temporal parameters were most strongly correlated with eye movement temporal metrics (head–eye-related burst neurons, HEBNs). These results suggest that FEF units do not encode a command for the unified gaze shift only; instead, different units may carry signals related to the overall gaze shift or its eye and/or head components. Moreover, the HEBNs exhibit bursts whose magnitude and timing may encode a head displacement signal and a signal that influences the timing of the eye saccade, thereby serving as a mechanism for coordinating the eye and head movements of a gaze shift.

Direct projections of omnipause neurons to reticulospinal neurons: A double‐labeling light microscopic study in the cat

Omnipause neurons (OPNs) are inhibitory neurons located in the midline region of the caudal pons. Their role in gating the discharges of saccade-related burst neurons is well known, but there is no agreement concerning their influence on brainstem neurons that control other muscle groups participating in rapid gaze shifts. In the present study, we inquired whether OPNs project directly to pontobulbar reticulospinal neurons (RSNs) in the cat. Retrograde transport of horseradish peroxidase from the cervical spinal cord was used to label RSNs and an anterograde tracer (biocytin) was iontophoresed at sites of extracellular recording of the OPN activity. Somadendritic characteristics of biocytin-labeled OPNs were largely similar to those obtained previously with intracellular labeling. Three-dimensional reconstruction of axonal trajectories and collaterals revealed that projections of OPNs, regarded as a population, are bilateral. Their terminals were restricted to the reticular formation and midline structures throughout the rostral bulbar and pontine tegmentum. Appositions of synaptic boutons originating from five fully stained OPNs were detected on 38 retrogradely labeled RSNs, each of the OPNs contacting 3-13 cells. The numbers of boutons (1-46; mean 11.8) on the RSN somata and proximal dendrites indicate that the anatomical strength of paired OPN-RSN connections is comparable to that of other similarly studied inhibitory neurons in the cat. The existence of connections with RSNs supports the hypothesis of a generalized influence of OPNs on several effectors participating in orienting gaze shifts as opposed to the idea of their strict specialization for the control of eye saccades.

The Locus of Motor Activity in the Superior Colliculus of the Rhesus Monkey Is Unaltered during Saccadic Adaptation

The location of motor-related activity in the deeper layers of the superior colliculus (SC) is thought to generate a desired displacement command specifying the amplitude and direction of saccadic eye movements. However, the amplitude of saccadic eye movements made to visual targets can be systematically altered by surreptitiously moving the target location after the saccade has been initiated. Depending on whether the target is moved closer to or further from the fixation location, adaptation of saccade amplitude results in movements that are either smaller or larger than control movements. It remains an open question whether the SC specifies the desired movement to the original target location or whether SC activity specifies the vector of the amplitude-altered movement that is observed as adaptation progresses. We investigated this question by recording the activity of saccade-related burst neurons in the SC of head-restrained rhesus monkeys during both backward and forward saccadic adaptation. During adaptation in each direction, we find no evidence that is consistent with a change in the locus of SC activity despite changes in saccade amplitude; the location of SC motor-related activity does not appear to be remapped during either forward or backward saccadic adaptation. These data are inconsistent with hypotheses that propose a key role for the SC in mediating the changes in saccade amplitude observed during adaptation.

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.

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.

Contribution of pedunculopontine tegmental nucleus neurons to performance of visually guided saccade tasks in monkeys.

The cholinergic pedunculopontine tegmental nucleus (PPTN) is one of the major ascending arousal systems in the brain stem and is linked to motor, limbic, and sensory systems. Based on previous studies, we hypothesized that PPTN would be related to the integrative control of movement, reinforcement, and performance of tasks in behaving animals. To investigate how PPTN contributes to the behavioral control, we analyzed the activity of PPTN neurons during visually guided saccade tasks in three monkeys in relation to saccade preparation, execution, reward, and performance of the task. During visually guided saccades, we observed saccade-related burst (26/70) and pause neurons (19/70), indicating that a subset of PPTN neurons are related to both saccade execution and fixation. Burst neurons exhibited greater selectivity for saccade direction than pause neurons. The preferred directions for both burst and pause neurons were not aligned with either horizontal or vertical axes, nor biased strongly in either the ipsilateral or the contralateral direction. The spatial representation of the saccade-related activity of PPTN neurons is different from other brain stem saccade systems and may therefore relay saccade-related activity from different areas. Increasing discharges were observed around reward onset in a subset of neurons (22/70). These neurons responded to the freely delivered rewards within ~140 ms. However, during the saccade task, the latencies of the responses around reward onset ranged between 100 ms before and 200 ms after the reward onset. These results suggest that the activity observed after appropriate saccade during the task may include response associated with reward. We found that the reaction time to the appearance of the fixation point (FP) was longer when the animal tended to fail in the ensuring task. This reaction time to FP appearance (RTFP) served as an index of motivation. The RTFP could be predicted by the neuronal activity of a subset of PPTN neurons (13/70) that varied their activity levels with task performance, discharging at a higher rate in successful versus error trials. A combination of responses related to saccade execution, reward delivery, and task performance was observed in PPTN neurons. We conclude from the multimodality of responses in PPTN neurons that PPTN may serve as an integrative interface between the various signals required for performing purposive behaviors.

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.

Ocular counterroll modulates the preferred direction of saccade-related pontine burst neurons in the monkey.

Saccade-related burst neurons in the paramedian pontine reticular formation (PPRF) of the head-restrained monkey provide a phasic velocity signal to extraocular motoneurons for the generation of rapid eye movements. In the superior colliculus (SC), which directly projects to the PPRF, the motor command for conjugate saccades with the head restrained in a roll position is represented in a reference frame in between oculocentric and space-fixed coordinates with a clear bias toward gravity. Here we studied the preferred direction of premotor burst neurons in the PPRF during static head roll to characterize their frame of reference with respect to head and eye position. In 59 neurons (short-lead, burst-tonic, and long-lead burst neurons), we found that the preferred direction of eye displacement of these neurons changed, relative to head-fixed landmarks, in the horizontal-vertical plane during static head roll. For the short-lead burst neurons and the burst-tonic group, the change was about one-fourth of the amount of ocular counterroll (OCR) and significantly different from a head-centered representation. In the long-lead burst neurons, the rotation of the preferred direction showed a larger trend of about one-half of OCR. During microelectrical stimulation of the PPRF (9 sites in 2 monkeys), the elicited eye movements rotated with about one-half the amount of OCR. In a simple pulley model of the oculomotor plant, the noncraniocentric reference frame of the PPRF output neurons could be reproduced for recently measured pulley positions, if the pulleys were assumed to rotate as a function of OCR with a gain of 0.5. We conclude that the saccadic displacement signal is transformed from a representation in the SC with a clear bias to gravity to a representation in the PPRF that is closely craniocentric, but rotates with OCR, consistent with current concepts of the oculomotor plant.

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.

Neurons in the primate superior colliculus coding for arm movements in gaze-related coordinates.

In the intermediate and deep layers of the superior colliculus (SC), a well-established oculomotor structure, a substantial population of cells is involved in the control of arm movements. To examine the reference frame of these neurons, we recorded in two rhesus monkeys (Macaca mulatta) the discharges of 331 neurons in the SC and the underlying mesencephalic reticular formation (MRF) while monkeys reached to the same target location during different gaze orientations. For 65 reach-related cells with sufficient data and for simultaneously recorded electromyograms (EMGs) of 11 arm muscles, we calculated an ANOVA (factors: target position, gaze angle) and a gaze-dependency (GD) index. EMGs and the activity of many (60%) of the reach-related neurons were not influenced by the target representation on the retina or eye position. We refer to these as "gaze-independent" reach neurons. For 40%, however, the GD fell outside the range of the muscle modulation, and the ANOVA showed a significant influence of gaze. These "gaze-related" reach neurons discharge only when the monkey reaches for targets having specific coordinates in relation to the gaze axis, i.e., for targets in a gaze-related "reach movement field" (RMF). Neuronal activity was not modulated by the specific path of the arm movement, the muscle pattern that is necessary for its realization or the arm that was used for the reach. In each SC we found gaze-related neurons with RMFs both in the contralateral and in the ipsilateral hemifield. The topographical organization of the gaze-related reach neurons in the SC could not be matched with the well-known visual and oculomotor maps. Gaze-related neurons were more modulated in their strength of activity with different directions of arm movements than were gaze-independent reach neurons. Gaze-related reach neurons were recorded at a median depth of 2.03 mm below SC surface in the intermediate layers, where they overlap with saccade-related burst neurons (median depth: 1.55 mm). Most of the gaze-independent reach cells were found in a median depth of 4.01 mm below the SC surface in the deep layers and in the underlying MRF. The gaze-related reach neurons operating in a gaze-centered coordinate system could signal either the desired target position with respect to gaze direction or the motor error between gaze axis and reach target. The gaze-independent reach neurons, possibly operating in a shoulder- or arm-centered reference frame, might carry signals closer to motor output. Together these two types of reach neurons add evidence to our hypothesis that the SC is involved in the sensorimotor transformation for eye-hand coordination in primates.

Activity in deep intermediate layer collicular neurons during interrupted saccades.

The activity of neurons located in the deep intermediate and adjacent deep layers (hereafter called just deep intermediate layer neurons) of the superior colliculus (SC) in monkeys was recorded during saccades interrupted by electrical stimulation of the brainstem omnipause neuron (OPN) region. The goal of the experiment was to determine if these neurons maintained their discharge during the saccadic interruption, and thus, could potentially provide a memory trace for the intended movement which ends accurately on target in spite of the perturbation. The collicular neurons recorded in the present study were located in the rostral three-fifths of the colliculus. Most of these cells tended to show considerable presaccadic activity during a delayed saccade paradigm, and, therefore, probably overlap with the population of SC cells called buildup neurons or prelude bursters in previous studies. The effect of electrical stimulation in the OPN region (which interrupted ongoing saccades) on the discharge of these neurons was measured by computing the percentage reduction in a cell's activity compared to that present during non-interrupted saccades. During saccade interruption about 70% of deep intermediate layer neurons experienced a major reduction (30% or greater) in their activity, but discharge recovered quickly after the termination of the stimulation as the eyes resumed their movement to finish the saccade on the target. Therefore, the pattern of activity recorded in most of the deep intermediate layer neurons during interrupted saccades qualitatively resembled that previously reported for the saccade-related burst neurons which tend to be located more dorsally in the intermediate layer. In contrast, some of our cells (30%) showed little or no perturbation in their activity caused by the saccade interrupting stimulation. Because all the more dorsally located burst neurons and the majority of our deep intermediate layer neurons show a total or major suppression in their discharge during interrupted saccades, it seems unlikely that the colliculus by itself could maintain an accurate memory of the desired saccadic goal or the remaining dynamic motor error required to account for the accuracy of the resumed movement which occurs following the interruption. However, it remains possible that the smaller proportion of our neurons whose activity was not perturbed during interrupted movements could play a role in the mechanisms underlying saccade accuracy in the interrupted saccade paradigm. Interrupted saccades have longer durations than normal saccades to the same target. Therefore, we investigated whether the discharge of our deeper collicular cells was also necessarily prolonged during interrupted saccades, and, if so, how the prolongation compared to the prolongation of the saccade. Sixty percent of our sample neurons showed a prolongation in discharge that was approximately the same as the prolongation in saccade duration (difference < 15 ms in magnitude). The, observation that temporal discharge in our neurons was perturbed to roughly match saccadic temporal perturbation suggests that dynamic feedback about ongoing saccadic motion is provided to the colliculus, but does not necessarily imply that this structure is the site responsible for the computation of dynamic motor error.

Visual-auditory interactions modulate saccade-related activity in monkey superior colliculus

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.

システムニューロサイエンス教育講座 １２． 上丘を含むＳａｃｃａｄｅ系のモデル

Extraocular motoneurons receive excitatory or inhibitory signals from saccade-related burst neurons in the brain stem during saccades. These premotor neurons are driven mainly by the superior collliculus in the midbrain. Neural models of the saccade system that include the superior colliculus are reviewed with regard to whether the superior colliculus is included in a local feedback loop of the saccade system and how a spatially encoded signal in the superior colliculus is transformed into a temporally encoded signal in the motoneurons.

Response properties of saccade-related burst neurons in the central mesencephalic reticular formation.

We studied the activity of saccade-related burst neurons in the central mesencephalic reticular formation (cMRF) in awake behaving monkeys. In experiment 1, we examined the activity of single neurons while monkeys performed an average of 225 delayed saccade trials that evoked gaze shifts having horizontal and vertical amplitudes between 2 and 20 degrees . All neurons studied generated high-frequency bursts of activity during some of these saccades. For each neuron, the duration and frequency of these bursts of activity reached maximal values when the monkey made movements within a restricted range of horizontal and vertical amplitudes. The onset of the movement followed the onset of the burst by the longest intervals for movements within a restricted range of horizontal and vertical amplitudes. The range of movements for which this interval was longest varied from neuron to neuron. Across the population, these ranges included nearly all contraversive saccades with horizontal and vertical amplitudes between 2 and 20 degrees. In experiment 2, we used the following task to examine the low-frequency prelude of activity that cMRF neurons generate before bursting: the monkey was required to fixate a light-emitting diode (LED) while two eccentric visual stimuli were presented. After a delay, the color of the fixation LED was changed, identifying one of the two eccentric stimuli as the saccadic target. After a final unpredictable delay, the fixation LED was extinguished and the monkey was reinforced for redirecting gaze to the identified saccadic target. Some cMRF neurons fired at a low frequency during the interval after the fixation LED changed color but before it was extinguished. For many neurons, the firing rate during this interval was related to the metrics of the movement the monkey made at the end of the trial and, to a lesser degree, to the location of the eccentric stimulus to which a movement was not directed.

Monkey superior colliculus activity during short-term saccadic adaptation.

This article concerns the neural mechanisms that underlie short-term saccadic adaptation in the rhesus monkey. By means of a consistent intrasaccadic target displacement, the relation between visual input and motor output was gradually changed in three monkeys, such that they made hypometric saccades. During this process, the activity of saccade-related burst neurons in the intermediate and deep layers of the Superior Colliculus (SC) was recorded in two of the monkeys. Our findings show that, like in humans, only saccades evoked within a restricted field around the adaptation target were adapted. However, unlike in humans, the kinematic properties of adapted saccades also changed systematically during the adaptation process. Typically, adapted saccades were slower and had a longer duration than would be expected on the basis of the main sequence for nonadapted visually guided movements. During adaptation, saccade-related activity of units in the SC remained appropriate for the saccade that was required to foveate the initial target, rather than for the saccade that was actually made. This means that adaptation caused a dissociation between SC activity and the ensuing saccade. Thus, the activity of the colliculus was better described in "required eye displacement coordinates" than in "actual eye displacement coordinates." Our data provide further evidence for the hypothesis that short-term saccadic adaptation acts at a level downstream from the SC, presumably at a stage that determines the kinematics of saccadic eye movements.

Functional dissociation within the cerebellum: motor execution and sensori-motor readiness

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.

1518 Functional dissociation within the cerebellum: motor execution and sensori-motor readiness

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.

Visuomotor and motor type saccade related purkinje cells in the cerebellar hemisphere of the monkey

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.

1516 Visuomotor and motor type saccade related purkinje cells in the cerebellar hemisphere of the monkey

This paper reports on single-unit activity of saccade-related burst neurons (SRBNs) in the intermediate and deep layers of the monkey superior colliculus (SC), evoked by bimodal sensory stimulation. Monkeys were trained to generate saccadic eye movements towards visual stimuli, in either a unimodal visual saccade task, or in a bimodal visual-auditory task. In the latter task, the monkeys were required to make an accurate saccade towards a visual target, while ignoring an auditory stimulus. The presentation of an auditory stimulus in temporal and spatial proximity of the visual target influenced neither the accuracy nor the kinematic properties of the evoked saccades. However, it had a significant effect on the activity of 90% (45/50) of the SRBNs. The motor-related burst increased significantly in some neurons, but was suppressed in others. In visual-movement cells, comparable bimodal interactions were observed in both the visually evoked burst and the movement-related burst. The large differences observed in the movement-related activity of SRBNs for identical saccades under different sensory conditions do not support the hypothesis that such cells encode dynamic motor error. The only behavioral parameter that was affected by the presentation of the auditory stimulus was saccade latency. Auditory stimulation caused saccade latency changes in the majority of the experiments. Meanwhile, the timing of peak collicular motor activity and saccade onset remained tightly coupled for all stimulus configurations. In addition, saccade latency varied as function of the distance between the stimuli in 36% of the recordings. Interestingly, the occurrence of a spatial latency effect covaried significantly with a similar spatial influence on the SRBNs firing rate. These cells were always most active in the bimodal task when both stimuli were in spatial register, but activity decreased with increasing stimulus separation.