Similarity in Neuronal Firing Regimes across Mammalian Species.

UNLABELLED: The architectonic subdivisions of the brain are believed to be functional modules, each processing parts of global functions. Previously, we showed that neurons in different regions operate in different firing regimes in monkeys. It is possible that firing regimes reflect differences in underlying information processing, and consequently the firing regimes in homologous regions across animal species might be similar. We analyzed neuronal spike trains recorded from behaving mice, rats, cats, and monkeys. The firing regularity differed systematically, with differences across regions in one species being greater than the differences in similar areas across species. Neuronal firing was consistently most regular in motor areas, nearly random in visual and prefrontal/medial prefrontal cortical areas, and bursting in the hippocampus in all animals examined. This suggests that firing regularity (or irregularity) plays a key role in neural computation in each functional subdivision, depending on the types of information being carried. SIGNIFICANCE STATEMENT: By analyzing neuronal spike trains recorded from mice, rats, cats, and monkeys, we found that different brain regions have intrinsically different firing regimes that are more similar in homologous areas across species than across areas in one species. Because different regions in the brain are specialized for different functions, the present finding suggests that the different activity regimes of neurons are important for supporting different functions, so that appropriate neuronal codes can be used for different modalities.

No-go neurons in the cerebellar oculomotor vermis and caudal fastigial nuclei: planning tracking eye movements.

The cerebellar dorsal vermis lobules VI-VII (oculomotor vermis) and its output region (caudal fastigial nuclei, cFN) are involved in tracking eye movements consisting of both smooth-pursuit and saccades, yet, the exact role of these regions in the control of tracking eye movements is still unclear. We compared the neuronal discharge of these cerebellar regions using a memory-based, smooth-pursuit task that distinguishes discharge related to movement preparation and execution from the discharge related to the processing of visual motion signals or their memory. Monkeys were required to pursue (i.e., go), or not pursue (i.e., no-go) in a cued direction, based on the memory of visual motion direction and go/no-go instructions. Most (>60 %) of task-related vermal Purkinje cells (P-cells) and cFN neurons discharged specifically during the memory period following no-go instructions; their discharge was correlated with memory of no-go instructions but was unrelated to eye movements per se during the action period of go trials. The latencies of no-go discharge of vermal P-cells and cFN neurons were similar, but were significantly longer than those of supplementary eye field (SEF) no-go neurons during an identical task. Movement-preparation signals were found in ~30 % of smooth-pursuit-related neurons in these cerebellar regions and some of them also carried visual memory signals. Our results suggest that no-go neurons are a newly revealed class of neurons, detected using the memory-based pursuit task, in the oculomotor vermis-cFN pathway and that this pathway contributes specifically to planning requiring the working memory of no-go instructions and preparation of tracking eye movements.

Neuronal activity in medial superior temporal area (MST) during memory-based smooth pursuit eye movements in monkeys.

We examined recently neuronal substrates for predictive pursuit using a memory-based smooth pursuit task that distinguishes the discharge related to memory of visual motion-direction from that related to movement preparation. We found that the supplementary eye fields (SEF) contain separate signals coding memory and assessment of visual motion-direction, decision not-to-pursue, and preparation for pursuit. Since medial superior temporal area (MST) is essential for visual motion processing and projects to SEF, we examined whether MST carried similar signals. We analyzed the discharge of 108 MSTd neurons responding to visual motion stimuli. The majority (69/108 = 64%) were also modulated during smooth pursuit. However, in nearly all (104/108 = 96%) of the MSTd neurons tested, there was no significant discharge modulation during the delay periods that required memory of visual motion-direction or preparation for smooth pursuit or not-to-pursue. Only 4 neurons of the 108 (4%) exhibited significantly higher discharge rates during the delay periods; however, their responses were non-directional and not instruction specific. Representative signals in the MSTd clearly differed from those in the SEF during memory-based smooth pursuit. MSTd neurons are unlikely to provide signals for memory of visual motion-direction or preparation for smooth pursuit eye movements.

Oscillatory eye movements resembling pendular nystagmus in normal juvenile macaques.

PURPOSE: Juvenile monkeys being trained on smooth-pursuit tasks exhibit ocular oscillations resembling pendular nystagmus. The purpose of this study was to analyze these oscillations, the effects of gabapentin on them, and responses of cerebellar floccular neurons to understand possible neuronal mechanisms. METHODS: Four monkeys were trained for horizontal and vertical smooth pursuit; in two, saccades were also tested. Frequency, peak-to-peak eye velocity, and amplitude of the ocular oscillations were measured. In one monkey, the effect of gabapentin on the oscillations was measured, and oscillation-related neuronal discharge was recorded in the cerebellar floccular region. RESULTS: Ocular oscillations, with features of pendular nystagmus, appeared early during training of both horizontal and vertical pursuit in all four monkeys. Although these oscillations were observed both in the direction of pursuit and orthogonally, the velocity and amplitude of oscillation were larger in the direction of pursuit, implicating pursuit mechanisms in their generation. Corrective saccades were often superimposed on the oscillations during pursuit and fixation. Gabapentin suppressed oscillations in the monkey tested. Recordings in the floccular region revealed a subset of neurons discharged during both the oscillations and corrective saccades. Many of them exhibited burst-tonic discharge during visually guided saccades, similar to discharge of brain stem burst-tonic neurons, suggesting contributions of the neural integrator to the oscillations. CONCLUSIONS: The developmentally transient ocular oscillations occurring in monkeys during pursuit training has properties resembling pendular nystagmus. Both smooth pursuit and a neural integrator may contribute to these ocular oscillations. Analysis using an efference-copy pursuit model supports the interpretation herein.

Neuronal activity in the caudal frontal eye fields of monkeys during memory-based smooth pursuit eye movements: comparison with the supplementary eye fields.

Recently, we examined the neuronal substrate of predictive pursuit during memory-based smooth pursuit and found that supplementary eye fields (SEFs) contain signals coding assessment and memory of visual motion direction, decision not-to-pursue ("no-go"), and preparation for pursuit. To determine whether these signals were unique to the SEF, we examined the discharge of 185 task-related neurons in the caudal frontal eye fields (FEFs) in 2 macaques. Visual motion memory and no-go signals were also present in the caudal FEF but compared with those in the SEF, the percentage of neurons coding these signals was significantly lower. In particular, unlike SEF neurons, directional visual motion responses of caudal FEF neurons decayed exponentially. In contrast, the percentage of neurons coding directional pursuit eye movements was significantly higher in the caudal FEF than in the SEF. Unlike SEF inactivation, muscimol injection into the caudal FEF did not induce direction errors or no-go errors but decreased eye velocity during pursuit causing an inability to compensate for the response delays during sinusoidal pursuit. These results indicate significant differences between the 2 regions in the signals represented and in the effects of chemical inactivation suggesting that the caudal FEF is primarily involved in generating motor commands for smooth-pursuit eye movements.

Activity of pursuit-related neurons in medial superior temporal area (MST) during static roll-tilt.

Recent studies have shown that rhesus macaques can perceive visual motion direction in earth-centered coordinates as accurately as humans. We tested whether coordinate frames representing smooth pursuit and/or visual motion signals in medial superior temporal area (MST) are earth centered to better understand its role in coordinating smooth pursuit. In 2 Japanese macaques, we compared preferred directions (re monkeys' head-trunk axis) of pursuit and/or visual motion responses of MSTd neurons while upright and during static whole-body roll-tilt. In the majority (41/51 = 80%) of neurons tested, preferred directions of pursuit and/or visual motion responses were not significantly different while upright and during 40° static roll-tilt. Preferred directions of the remaining 20% of neurons (n = 10) were shifted beyond the range expected from ocular counter-rolling; the maximum shift was 14°, and the mean shift was 12°. These shifts, however, were still less than half of the expected shift if MST signals are coded in the earth-centered coordinates. Virtually, all tested neurons (44/46 = 96%) failed to exhibit a significant difference between resting discharge rate while upright and during static roll-tilt while fixating a stationary spot. These results suggest that smooth pursuit and/or visual motion signals of MST neurons are not coded in the earth-centered coordinates; our results favor the head- and/or trunk-centered coordinates.

Representation of neck velocity and neck-vestibular interactions in pursuit neurons in the simian frontal eye fields.

The smooth pursuit system must interact with the vestibular system to maintain the accuracy of eye movements in space (i.e., gaze-movement) during head movement. Normally, the head moves on the stationary trunk. Vestibular signals cannot distinguish whether the head or whole body is moving. Neck proprioceptive inputs provide information about head movements relative to the trunk. Previous studies have shown that the majority of pursuit neurons in the frontal eye fields (FEF) carry visual information about target velocity, vestibular information about whole-body movements, and signal eye- or gaze-velocity. However, it is unknown whether FEF neurons carry neck proprioceptive signals. By passive trunk-on-head rotation, we tested neck inputs to FEF pursuit neurons in 2 monkeys. The majority of FEF pursuit neurons tested that had horizontal preferred directions (87%) responded to horizontal trunk-on-head rotation. The modulation consisted predominantly of velocity components. Discharge modulation during pursuit and trunk-on-head rotation added linearly. During passive head-on-trunk rotation, modulation to vestibular and neck inputs also added linearly in most neurons, although in half of gaze-velocity neurons neck responses were strongly influenced by the context of neck rotation. Our results suggest that neck inputs could contribute to representing eye- and gaze-velocity FEF signals in trunk coordinates.

Reafferent head-movement signals carried by pursuit neurons of the simian frontal eye fields during head movements.

The smooth-pursuit system is important to precisely track a slowly moving object and maintain its image on the foveae during movement. During whole-body rotation, the smooth-pursuit system interacts with the vestibular system. The caudal part of the frontal eye fields (FEF) contains smooth pursuit-related neurons that signal eye velocity during pursuit. The majority of them receives vestibular inputs and signal gaze-velocity during passive whole-body rotation. It was asked whether discharge modulation of FEF pursuit neurons during head rotation on the stationary trunk could be accounted for by vestibular inputs only or if both vestibular and neck proprioceptive inputs contributed to the modulation. Discharge modulation during active head pursuit, passive head rotation on the stationary trunk, passive whole-body rotation, and passive trunk rotation against the stationary head were compared. The results indicate that both vestibular and neck proprioceptive inputs contributed to the discharge modulation of FEF pursuit neurons during head movements.

Relating neuronal firing patterns to functional differentiation of cerebral cortex.

It has been empirically established that the cerebral cortical areas defined by Brodmann one hundred years ago solely on the basis of cellular organization are closely correlated to their function, such as sensation, association, and motion. Cytoarchitectonically distinct cortical areas have different densities and types of neurons. Thus, signaling patterns may also vary among cytoarchitectonically unique cortical areas. To examine how neuronal signaling patterns are related to innate cortical functions, we detected intrinsic features of cortical firing by devising a metric that efficiently isolates non-Poisson irregular characteristics, independent of spike rate fluctuations that are caused extrinsically by ever-changing behavioral conditions. Using the new metric, we analyzed spike trains from over 1,000 neurons in 15 cortical areas sampled by eight independent neurophysiological laboratories. Analysis of firing-pattern dissimilarities across cortical areas revealed a gradient of firing regularity that corresponded closely to the functional category of the cortical area; neuronal spiking patterns are regular in motor areas, random in the visual areas, and bursty in the prefrontal area. Thus, signaling patterns may play an important role in function-specific cerebral cortical computation.

Memory and decision making in the frontal cortex during visual motion processing for smooth pursuit eye movements.

Cortical motor areas are thought to contribute "higher-order processing," but what that processing might include is unknown. Previous studies of the smooth pursuit-related discharge of supplementary eye field (SEF) neurons have not distinguished activity associated with the preparation for pursuit from discharge related to processing or memory of the target motion signals. Using a memory-based task designed to separate these components, we show that the SEF contains signals coding retinal image-slip-velocity, memory, and assessment of visual motion direction, the decision of whether to pursue, and the preparation for pursuit eye movements. Bilateral muscimol injection into SEF resulted in directional errors in smooth pursuit, errors of whether to pursue, and impairment of initial correct eye movements. These results suggest an important role for the SEF in memory and assessment of visual motion direction and the programming of appropriate pursuit eye movements.

Discharge of pursuit neurons in the caudal part of the frontal eye fields during cross-axis vestibular-pursuit training in monkeys.

Previous studies in monkeys have shown that pursuit training during orthogonal whole body rotation results in task-dependent, predictive pursuit eye movements. We examined whether pursuit neurons in the frontal eye fields (FEF) are involved in predictive pursuit induced by vestibular-pursuit training. Two monkeys were rotated horizontally at 20 degrees/s for 0.5 s either rightward or leftward with random inter-trial intervals. This chair motion trajectory was synchronized with orthogonal target motion at 20 degrees/s for 0.5 s either upward or downward. Monkeys were rewarded for pursuing the target. Vertical pursuit eye velocities and discharge of 23 vertical pursuit neurons to vertical target motion were compared before training and during the last 5 min of the 25-45 min training. The latencies of discharge modulation of 61% of the neurons (14/23) shortened after vestibular-pursuit training in association with a shortening of pursuit latency. However, their discharge modulation occurred after 100 ms following the onset of pursuit eye velocity. Only four neurons (4/23 = 17%) discharged before the eye movement onset. A significant change was not observed in eye velocity and FEF pursuit neuron discharge during pursuit alone after training without vestibular stimulation. Vestibular stimulation alone without a target after training induced no clear response. These results suggest that the adaptive change in response to pursuit prediction was induced by vestibular inputs in the presence of target pursuit. FEF pursuit neurons are unlikely to be involved in the initial stage of generating predictive eye movements. We suggest that they may participate in the maintenance of predictive pursuit.

Otolith inputs to pursuit neurons in the frontal eye fields of alert monkeys.

The smooth-pursuit system must interact with the vestibular system to maintain the accuracy of eye movements in space during head movement. Maintenance of a target image on the foveae is required not only during head rotation which activates primarily semi-circular canals but also during head translation which activates otolith organs. The caudal part of the frontal eye fields (FEF) contains pursuit neurons. The majority of them receive vestibular inputs induced by whole body rotation. However, it has not been tested whether FEF pursuit neurons receive otolith inputs. In the present study, we first classified FEF pursuit neurons as belonging to one of three groups (vergence + fronto-parallel pursuit, vergence only, fronto-parallel pursuit only) based on their responses during fronto-parallel pursuit and mid-sagittal vergence-pursuit. We, then, tested discharge modulation of these neurons during fore/aft and/or right/left translation by passively moving the whole body sinusoidally at 0.33 Hz (+/-10 cm, peak velocity 19 cm/s; 0.04g). The majority of FEF pursuit neurons in all three groups were activated by fore/aft and right/left translation without a target in complete darkness. There was no correlation between the magnitude of discharge modulation and translational vestibulo-ocular reflex (VOR). Preferred directions of translational responses were distributed nearly evenly in front of the monkeys. Discharge modulation was also observed when a target moved together with whole body, requiring the monkeys to cancel the translational VOR. These results indicate that the discharge modulation of FEF pursuit neurons during whole body translation reflected otolith inputs.

Discharge of pursuit-related neurons in the caudal part of the frontal eye fields in juvenile monkeys with up-down pursuit asymmetry.

The smooth-pursuit system uses retinal image-slip-velocity information of target motion to match eye velocity to actual target velocity. The caudal part of the frontal eye fields (FEF) contains neurons whose activity is related to direction and velocity of smooth-pursuit eye movements (pursuit neurons), and these neurons are thought to issue a pursuit command. During normal pursuit in well-trained adult monkeys, a pursuit command is usually not differentiable from the actual eye velocity. We examined whether FEF pursuit neurons signaled the actual eye velocity during pursuit in juvenile monkeys that exhibited intrinsic differences between upward and downward pursuit capabilities. Two, head-stabilized Japanese monkeys of 4 years of age were tested for sinusoidal vertical pursuit of target motion at 0.2-1.2 Hz (+/-10 degrees, peak target velocity 12.5-75.0 degrees/s). Gains of downward pursuit were 0.8-0.9 at 0.2-1.0 Hz, and peak downward eye velocity increased up to approximately 60 degrees/s linearly with target velocity, whereas peak upward eye velocity saturated at 15-20 degrees/s. The majority of downward FEF pursuit neurons increased the amplitude of their discharge modulation almost linearly up to 1.2 Hz. The majority of upward FEF pursuit neurons also increased amplitude of modulation nearly linearly as target frequency increased, and the regression slope was similar to that of downward pursuit neurons despite the fact that upward peak eye velocity saturated at approximately 0.5 Hz. These results indicate that the responses of the majority of upward FEF pursuit neurons did not signal the actual eye velocity during pursuit. We suggest that their activity reflected primarily the required eye velocity.

Eye-pursuit and reafferent head movement signals carried by pursuit neurons in the caudal part of the frontal eye fields during head-free pursuit.

Eye and head movements are coordinated during head-free pursuit. To examine whether pursuit neurons in frontal eye fields (FEF) carry gaze-pursuit commands that drive both eye-pursuit and head-pursuit, monkeys whose heads were free to rotate about a vertical axis were trained to pursue a juice feeder with their head and a target with their eyes. Initially the feeder and target moved synchronously with the same visual angle. FEF neurons responding to this gaze-pursuit were tested for eye-pursuit of target motion while the feeder was stationary and for head-pursuit while the target was stationary. The majority of pursuit neurons exhibited modulation during head-pursuit, but their preferred directions during eye-pursuit and head-pursuit were different. Although peak modulation occurred during head movements, the onset of discharge usually was not aligned with the head movement onset. The minority of neurons whose discharge onset was so aligned discharged after the head movement onset. These results do not support the idea that the head-pursuit-related modulation reflects head-pursuit commands. Furthermore, modulation similar to that during head-pursuit was obtained by passive head rotation on stationary trunk. Our results suggest that FEF pursuit neurons issue gaze or eye movement commands during gaze-pursuit and that the head-pursuit-related modulation primarily reflects reafferent signals resulting from head movements.

Vergence eye movement signals in the cerebellar dorsal vermis.

We examined simple-spike activity of Purkinje cells (P-cells) that responded during a search task which required both vergence- and frontal-pursuit. Of a total of 100 responding P-cells, 16% discharged only for frontal-pursuit, 43% only for vergence-pursuit, and 41% for both. Thus, the majority of vermal pursuit P-cells modulated their activity during vergence-pursuit. These P-cells also discharged for vergence eye movements induced by step target-motion in-depth. The majority of vergence related P-cells carried convergence signals with both eye velocity and position sensitivities, and they discharged before the onset of convergence eye movements. Muscimol infusion into the sites where convergence P-cells were recorded resulted in a reduction of peak convergence eye velocity, of initial convergence eye acceleration, and of frontal-pursuit eye velocity. These results suggest specific involvement of the dorsal vermis in vergence eye movements.

Involvement of the cerebellar dorsal vermis in vergence eye movements in monkeys.

Frontal-eyed primates use both smooth pursuit in frontoparallel planes (frontal pursuit) and pursuit-in-depth (vergence pursuit) to track objects moving slowly in 3-dimensional (3D) space. To understand how 3D-pursuit signals represented in frontal eye fields are processed further by downstream pathways, monkeys were trained to pursue a spot moving in 3D virtual space. We characterized pursuit signals in Purkinje (P) cells in the cerebellar dorsal vermis and their discharge during vergence pursuit. In 41% of pursuit P-cells, 3D-pursuit signals were observed. However, the majority of vermal-pursuit P-cells (59%) discharged either for vergence pursuit (43%) or for frontal pursuit (16%). Moreover, the majority (74%) of vergence-related P-cells carried convergence signals, displaying both vergence eye position and velocity sensitivity during sinusoidal and step vergence eye movements. Preferred frontal-pursuit directions of vergence + frontal-pursuit P-cells were distributed in all directions. Most pursuit P-cells (73%) discharged before the onset of vergence eye movements; the median lead time was 16 ms. Muscimol infusion into the sites where convergence P-cells were recorded resulted in a reduction of peak convergence eye velocity, of initial convergence eye acceleration, and of frontal-pursuit eye velocity. These results suggest involvement of the dorsal vermis in conversion of 3D-pursuit signals and in convergence eye movements.

Directional asymmetry in vertical smooth-pursuit and cancellation of the vertical vestibulo-ocular reflex in juvenile monkeys.

Young primates exhibit asymmetric eye movements during vertical smooth-pursuit across a textured background such that upward pursuit has low velocity and requires many catch-up saccades. The asymmetric eye movements cannot be explained by the un-suppressed optokinetic reflex resulting from background visual motion across the retina during pursuit, suggesting that the asymmetry reflects most probably, a low gain in upward eye commands (Kasahara et al. in Exp Brain Res 171:306-321, 2006). In this study, we examined (1) whether there are intrinsic differences in the upward and downward pursuit capabilities and (2) how the difficulty in upward pursuit is correlated with the ability of vertical VOR cancellation. Three juvenile macaques that had initially been trained only for horizontal (but not vertical) pursuit were trained for sinusoidal pursuit in the absence of a textured background. In 2 of the 3 macaques, there was a clear asymmetry between upward and downward pursuit gains and in the time course of initial gain increase. In the third macaque, downward pursuit gain was also low. It did not show consistent asymmetry during the initial 2 weeks of training. However, it also exhibited a significant asymmetry after 4 months of training, similar to the other two monkeys. After 6 months of training, these two monkeys (but not the third) still exhibited asymmetry. As target frequency increased in these two monkeys, mean upward eye velocity saturated at approximately 15 degrees /s, whereas horizontal and downward eye velocity increased up to approximately 40 degrees /s. During cancellation of the VOR induced by upward whole body rotation, downward eye velocity of the residual VOR increased as the stimulus frequency increased. Gain of the residual VOR during upward rotation was significantly higher than that during horizontal and downward rotation. The time course of residual VOR induced by vertical whole body step-rotation during VOR cancellation was predicted by addition of eye velocity during pursuit and VOR x1. These results support our view that the directional asymmetry reflects the difference in the organization of the cerebellar floccular region for upward and downward directions and the preeminent role of pursuit in VOR cancellation.

Activity of pursuit neurons in the caudal part of the frontal eye fields during static roll-tilt.

The smooth-pursuit system and vestibular system interact to keep the retinal target image on the fovea during head and/or whole body movements. The caudal part of the frontal eye fields (FEF) in the fundus of arcuate sulcus contains pursuit neurons and the majority of them respond to vestibular stimulation induced by whole-body rotation, that activates primarily semi-circular canals, and by whole-body translation, that activates otoliths. To examine whether coordinate frames representing FEF pursuit signals are orbital or earth-vertical, we compared preferred directions during upright and static, whole-body roll-tilt in head- and trunk-restrained monkeys. Preferred directions (re monkeys' head/trunk axis) of virtually all pursuit neurons tested (n = 21) were similar during upright and static whole-body roll-tilt. The slight shift of preferred directions of the majority of neurons could be accounted for by ocular counter-rolling. The mean (+/-SD) differences in preferred directions between upright and 40 degrees right ear down and between upright and 40 degrees left ear down were 6 degrees (+/-6 degrees) and 5 degrees (+/-5 degrees), respectively. Visual motion preferred directions were also similar in five pursuit neurons tested. To examine whether FEF pursuit neurons could signal static whole-body roll-tilt, we compared mean discharge rates of 29 neurons during fixation of a stationary spot while upright and during static, whole-body roll-tilt. Virtually all neurons tested (28/29) did not exhibit a significant difference in mean discharge rates between the two conditions. These results suggest that FEF pursuit neurons do not signal static roll-tilt and that they code pursuit signals in head/trunk-centered coordinates.

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation.

The smooth pursuit system and the vestibular system interact to keep the retinal target image on the fovea by matching the eye velocity in space to target velocity during head and/or whole body movement. The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains pursuit-related neurons and the majority of them respond to vestibular stimulation induced by whole body movement. To understand the role of FEF pursuit neurons in the interaction of vestibular and pursuit signals, we examined the latency and time course of discharge modulation to horizontal whole body rotation during different vestibular task conditions in head-stabilized monkeys. Pursuit neurons with horizontal preferred directions were selected, and they were classified either as gaze-velocity neurons or eye/head-velocity neurons based on the previous criteria. Responses of these neurons to whole body step-rotation at 20 degrees/s were examined during cancellation of the vestibulo-ocular reflex (VOR), VOR x1, and during chair steps in complete darkness without a target (VORd). The majority of pursuit neurons tested (approximately 70%) responded during VORd with latencies <80 ms. These initial responses were basically similar in the three vestibular task conditions. The shortest latency was 20 ms and the modal value was 24 ms. These responses were also similar between gaze-velocity neurons and eye/head-velocity neurons, indicating that the initial responses (<80 ms) were vestibular responses induced by semicircular canal inputs. During VOR cancellation and x1, discharge of the two groups of neurons diverged at approximately 90 ms following the onset of chair rotation, consistent with the latencies associated with smooth pursuit. The shortest latency to the onset of target motion during smooth pursuit was 80 ms and the modal value was 95 ms. The time course of discharge rate difference of the two groups of neurons between VOR cancellation and x1 was predicted by the discharge modulation associated with smooth pursuit. These results provide further support for the involvement of the caudal FEF in integration of vestibular inputs and pursuit signals.

The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions.

In order to see clearly when a target is moving slowly, primates with high acuity foveae use smooth-pursuit and vergence eye movements. The former rotates both eyes in the same direction to track target motion in frontal planes, while the latter rotates left and right eyes in opposite directions to track target motion in depth. Together, these two systems pursue targets precisely and maintain their images on the foveae of both eyes. During head movements, both systems must interact with the vestibular system to minimize slip of the retinal images. The primate frontal cortex contains two pursuit-related areas; the caudal part of the frontal eye fields (FEF) and supplementary eye fields (SEF). Evoked potential studies have demonstrated vestibular projections to both areas and pursuit neurons in both areas respond to vestibular stimulation. The majority of FEF pursuit neurons code parameters of pursuit such as pursuit and vergence eye velocity, gaze velocity, and retinal image motion for target velocity in frontal and depth planes. Moreover, vestibular inputs contribute to the predictive pursuit responses of FEF neurons. In contrast, the majority of SEF pursuit neurons do not code pursuit metrics and many SEF neurons are reported to be active in more complex tasks. These results suggest that FEF- and SEF-pursuit neurons are involved in different aspects of vestibular-pursuit interactions and that eye velocity coding of SEF pursuit neurons is specialized for the task condition.