Role of the cerebellar flocculus region in the coordination of eye and head movements during gaze pursuit

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive ( approximately 43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.     

Reorientation of a visually evoked postural response during passive whole body rotation

Visually evoked postural responses (VEPR) to a roll-motion rotating disk were recorded from normal subjects standing on a yaw axis motorised rotating platform. The disk was fluorescent so that subjects could be tested in an otherwise dark room. Movements of the head and centre of foot pressure were measured while subjects looked at the disk with their eyes and head in the primary position and while the rotating platform moved the subjects randomly to 0, +/-45 degrees and +/-90 degrees angles from the visual stimulus. Subjects were instructed to maintain fixation on the centre of the rotating disk but the amount of horizontal eye and head movement used was not specified. Platform rotational velocity was set near threshold values for perception of self-rotation (approximately 2 degrees/s) so that subjects would find it difficult to reconstruct the angle travelled. The data showed that the VEPR occurred in the plane of disk rotation, regardless of body position with respect to the disk, and despite the subjective spatial disorientation induced by the experiment. Averages of the response revealed a good match (gain=0.95) between disk orientation and sway direction. The horizontal gaze deviation required to fixate the centre of the disk was largely achieved by head motion (head 95%, eye 5%). The results confirm previous results that VEPRs are reoriented according to horizontal gaze angle. In addition, we show that the postural reorientation is independent of cognitively or visually mediated knowledge of the geometry of the experimental conditions. In the current experiments, the main source of gaze position input required for VEPR reorientation was likely to be provided by neck afferents. The results support the notion that vision controls posture effectively at any gaze angle and that this is achieved by combining visual input with proprioceptively mediated gaze-angle signals.     

Pursuit-related neurons in the supplementary eye fields: discharge during pursuit and passive whole body rotation

The primate frontal cortex contains two areas related to smooth-pursuit: the frontal eye fields (FEFs) and supplementary eye fields (SEFs). To distinguish the specific role of the SEFs in pursuit, we examined discharge of a total of 89 pursuit-related neurons that showed consistent modulation when head-stabilized Japanese monkeys pursued a spot moving sinusoidally in fronto-parallel planes and/or in depth and with or without passive whole body rotation. During smooth-pursuit at different frequencies, 43% of the neurons tested (17/40) exhibited discharge amplitude of modulation linearly correlated with eye velocity. During cancellation of the vestibulo-ocular reflex and/or chair rotation in complete darkness, the majority of neurons tested (91% = 30/33) responded. However, only 17% of the responding neurons (4/30) were modulated in proportion to gaze (eye-in-space) velocity during pursuit-vestibular interactions. When the monkeys fixated a stationary spot, 20% of neurons tested (7/34) responded to motion of a second spot. Among the neurons tested for both smooth-pursuit and vergence tracking (n = 56), 27% (15/56) discharged during both, 62% (35/56) responded during smooth-pursuit only, and 11% (6/56) during vergence tracking only. Phase shifts (relative to stimulus velocity) of responding neurons during pursuit in frontal and depth planes and during chair rotation remained virtually constant (< or =1 Hz). These results, together with the robust vestibular-related discharge of most SEF neurons, show that the discharge of the majority of SEF pursuit-related neurons is quite distinct from that of caudal FEF neurons in identical task conditions, suggesting that the two areas are involved in different aspects of pursuit-vestibular interactions including predictive pursuit.     

Galvanic stimulation of the vestibular periphery in guinea pigs during passive whole body rotation and self-generated head movement

Irregular vestibular afferents exhibit significant phase leads with respect to angular velocity of the head in space. This characteristic and their connectivity with vestibulospinal neurons suggest a functionally important role for these afferents in producing the vestibulo-collic reflex (VCR). A goal of these experiments was to test this hypothesis with the use of weak galvanic stimulation of the vestibular periphery (GVS) to selectively activate or suppress irregular afferents during passive whole body rotation of guinea pigs that could freely move their heads. Both inhibitory and excitatory GVS had significant effects on compensatory head movements during sinusoidal and transient whole body rotations. Unexpectedly, GVS also strongly affected the vestibulo-ocular reflex (VOR) during passive whole body rotation. The effect of GVS on the VOR was comparable in light and darkness and whether the head was restrained or unrestrained. Significantly, there was no effect of GVS on compensatory eye and head movements during volitional head motion, a confirmation of our previous study that demonstrated the extravestibular nature of anticipatory eye movements that compensate for voluntary head movements.     

Vertical Purkinje cells of the monkey floccular lobe: simple-spike activity during pursuit and passive whole body rotation.

To understand how the simian floccular lobe is involved in vertical smooth pursuit eye movements and the vertical vestibuloocular reflex (VOR), we examined simple-spike activity of 70 Purkinje (P) cells during pursuit eye movements and passive whole body rotation. Fifty-eight cells responded during vertical and 12 during horizontal pursuit. We classified P cells as vertical gaze velocity (VG) if their modulation occurred for movements of both the eye (during vertical pursuit) and head (during pitch VOR suppression) with the modulation during one less than twice that of the other and was less during the target-fixed-in-space condition (pitch VOR X1) than during pitch VOR suppression. VG P cells constituted only a minority of vertical P cells (19%). Other vertical P cells that responded during pitch VOR suppression were classified as vertical eye and head velocity (V/) P cells (48%), regardless of the synergy of their response direction during smooth pursuit and VOR suppression. Vertical P cells that did not respond during pitch VOR suppression but did respond during rotation in vertical planes other than pitch were classified as off-pitch V/ P cells (33%). The mean eye-velocity and eye-position sensitivities of the three types of vertical P cells were similar. One-third (2/7 VG, 2/11 V/, 6/13 off-pitch V/), in addition, showed eye position sensitivity during saccade-free fixations. Maximal vestibular activation directions (MADs) were examined during VOR suppression by applying vertical whole body rotation with the monkeys oriented in different vertical planes. The MADs for VG P cells and V/ P cells with eye and vestibular sensitivity in the same direction were distributed near the pitch plane, suggesting convergence of bilateral anterior canal inputs. In contrast, MADs of off-pitch V/ P cells and V/ P cells with oppositely directed eye and vestibular sensitivity were shifted toward the roll plane, suggesting convergence of anterior and posterior canal inputs of the same side. Unlike horizontal G P cells, the modulation of many VG and V/ P cells when the target was fixed in space (pitch VOR X1) was not well predicted by the linear addition of their modulations during vertical pursuit and pitch VOR suppression. These results indicate that the populations of vertical and horizontal eye-movement P cells in the floccular lobe have markedly different discharge properties and therefore may be involved in different kinds of processing of vestibular-oculomotor interactions.     

Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI-VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR x1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR x1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.     

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation.

1. Extracellular recordings were obtained from 124 Purkinje cells (P-cells) in the flocculus of alert monkeys. P-cell simple spike-firing rate was analyzed quantitatively during various combinations of smooth-pursuit eye movement and passive head rotation. 2. During sinusoidal smooth eye movements, 80% of the P-cells displayed increased firing rate during ipsilateral and 20% during contralateral eye movement. Over the frequency range 0.3--1.4 Hz, firing-rate modulation was proportional to and in phase with maximum eye velocity. During the steady state of triangle-wave tracking, firing rate increased monotonically as a function of eye velocity. Since firing rate was uncorrelated with retinal-error velocity, one component of P-cell firing rate was related to eye velocity. 3. During the transient phase of triangle-wave tracking, when an instantaneous change in the direction of target movement caused a large retinal-error velocity, 40% of the P-cells were related only to eye velocity. Sixty percent of the P-cells displayed an overshoot or undershoot in firing rate, indicating a relationship to either retinal-error velocity or eye acceleration as well as to eye velocity. 4. During the vestibuloocular reflex (VOR), evoked by head rotation in the dark, P-cell firing rate was only weakly modulated. In contrast, when the monkey suppressed the VOR by fixating a target that rotated with him, P-cell rate was deeply modulated. Since the modulation was proportional to and in phase with maximum head velocity, another component of P-cell firing rate was related to head velocity. 5. Of 36 P-cells tested, 35 displayed firing-rate modulation during both suppression of the VOR and smooth-pursuit eye movement. P-cells that reached peak firing rate during ipsilateral head rotation also reached peak firing rate during ipsilateral smooth eye rotation. Average population sensitivitites to head velocity and eye velocity were equal. In three conditions in which eye and head velocity were elicited simultaneously, P-cell firing rate could be predicted by the linear, vector addition of the separate eye and head velocity components of firing rate. Therefore, the relatively weak modulation of P-cell firing rate during the VOR in the dark can be accounted for by the cancellation of equal but opposite head and eye velocity components. 6. The connections of flocculus P-cells to interneurons in the brain stem VOR pathways have been established in other mammals. In the context of those connections, P-cell firing patterns were appropriate to facilitate the eye movements the monkey was required to make. We conclude that the flocculus is important for sustaining any smooth eye movements that are different from those evoked by head rotation in the dark. The eye velocity component may represent an efference copy signal that sustains ongoing eye velocity during smooth pursuit.     

Motor learning in the VOR: the cerebellar component

This paper reviews results that support a model in which memory for VOR gain is initially encoded in the flocculus, and in which cerebellar LTD and LTP are responsible for gain increases and gain decreases, respectively. We also review data suggesting that after it is encoded, motor memory can either be disrupted, possibly by a local mechanism, or else consolidated. We show that consolidation can be rapid, in which case the frequency dependence of learning is unchanged and we will argue that this is consistent with a local mechanism of consolidation. In the longer term, however, the available evidence supports the transfer of memory out of the flocculus. In new experiments reported here, we address the mechanism of memory encoding. Pharmacological evidence shows that both mGluR1 and GABA_B receptors in the flocculus are necessary for gain-up, but not for gain-down learning. Immunohistochemical experiments show that the two receptors are largely segregated on different dendritic spines on Purkinje cells. Together with what is already known of the mechanisms of cerebellar LTD and LTP, our data suggest that the direction of learning may be determined by interactions among groups of spines. Our results also provide new evidence for the existence of frequency channels for vestibular signals within the cerebellar cortex.     

Injections of beta-noradrenergic substances in the flocculus of rabbits affect adaptation of the VOR gain

Noradrenaline (NA) has been implicated as a neuromodulator in plasticity, presumably facilitating adaptive processes. Recent experiments by others have suggested a modulatory role of NA in adaptive changes in the vestibulo-ocular reflex (VOR). These experiments showed that general depletion of brain NA resulted in a decreased ability to produce adaptive changes in the VOR gain. In order to identify the specific brain region responsible for these effects, as well as the nature of the adrenoceptors involved, we injected beta-adrenergic substances bilaterally into the flocculus of rabbits. The flocculus is known to receive noradrenergic afferents and, moreover, ablation of the flocculus interferes strongly with the normal adaptive changes in the VOR gain. We injected the beta-agonist isoproterenol and the beta-antagonist sotalol, and compared the adaptive capacity of the rabbits after these injections to that in a situation without injection. The rabbit was oscillated in a direction opposite to the direction of motion of the platform on which the rabbit was mounted, a condition which normally results in an increase in the VOR gain, measured either in light or in darkness. Injection of the beta-agonist did not greatly affect the adaptation of the VOR measured in the light. In darkness, the increase in gain after the injection of isoproterenol was larger than in the non-injection experiments in 9 out of 10 rabbits. The beta-antagonist sotalol reduced the adaptation of the VOR gain significantly in the light, as well as in darkness. In a control condition without pressure for adaptation (only intermittent testing of the VOR gain over a period of 2.5 h), the gain of the VOR either remained unaffected or was only slightly affected by similar injections of beta-adrenergic agents in individual rabbits. For the group as a whole, these effects were insignificant. We conclude from these results that noradrenergic systems facilitate the adaptation of the VOR gain to retinal slip in rabbits, without affecting the VOR gain directly. At least part of this influence is exerted through beta-receptors located in the cerebellar flocculus.     

Contribution of the cerebellar flocculus to gaze control during active head movements.

The flocculus and ventral paraflocculus are adjacent regions of the cerebellar cortex that are essential for controlling smooth pursuit eye movements and for altering the performance of the vestibulo-ocular reflex (VOR). The question addressed in this study is whether these regions of the cerebellum are more globally involved in controlling gaze, regardless of whether eye or active head movements are used to pursue moving visual targets. Single-unit recordings were obtained from Purkinje (Pk) cells in the floccular region of squirrel monkeys that were trained to fixate and pursue small visual targets. Cell firing rate was recorded during smooth pursuit eye movements, cancellation of the VOR, combined eye-head pursuit, and spontaneous gaze shifts in the absence of targets. Pk cells were found to be much less sensitive to gaze velocity during combined eye-head pursuit than during ocular pursuit. They were not sensitive to gaze or head velocity during gaze saccades. Temporary inactivation of the floccular region by muscimol injection compromised ocular pursuit but had little effect on the ability of monkeys to pursue visual targets with head movements or to cancel the VOR during active head movements. Thus the signals produced by Pk cells in the floccular region are necessary for controlling smooth pursuit eye movements but not for coordinating gaze during active head movements. The results imply that individual functional modules in the cerebellar cortex are less involved in the global organization and coordination of movements than with parametric control of movements produced by a specific part of the body.     

Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades

The vestibuloocular reflex (VOR) functions to stabilize gaze when the head moves. The flocculus region (FLR) of the cerebellar cortex, which includes the flocculus and ventral paraflocculus, plays an essential role in modifying signal processing in VOR pathways so that images of interest remain stable on the retina. In squirrel monkeys, the firing rate of most FLR Pk cells is modulated during VOR eye movements evoked by passive movement of the head. In this study, the responses of 48 FLR Purkinje cells, the firing rates of which were strongly modulated during VOR evoked by passive whole body rotation or passive head-on-trunk rotation, were compared to the responses generated during compensatory VOR eye movements evoked by the active head movements of eye-head saccades. Most (42/48) of the Purkinje cells were insensitive to eye-head saccade-related VOR eye movements. A few (6/48) generated bursts of spikes during saccade-related VOR but only during on-direction eye movements. Considered as a population FLR Pk cells were <5% as responsive to the saccade-related VOR as they were to the VOR evoked by passive head movements. The observations suggest that the FLR has little influence on signal processing in VOR pathways during eye-head saccade-related VOR eye movements. We conclude that the image-stabilizing signals generated by the FLR are highly dependent on the behavioral context and are called on primarily when external forces unrelated to self-generated eye and head movements are the cause of image instability.     

Motor dynamics encoding in cat cerebellar flocculus middle zone during optokinetic eye movements

We investigated the relationship between eye movement and simple-spike (SS) frequency of Purkinje cells in the cerebellar flocculus middle zone during the optokinetic response (OKR) in alert cats. The OKR was elicited by a sequence of a constant-speed visual pattern movement in one direction for 1 s and then in the opposite direction for 1 s. Quick-phase-free trials were selected. Sixty-six cells had direction-selective complex spike (CS) activity that was modulated during horizontal (preferring contraversive) but not vertical stimuli. The SS activity was modulated during horizontal OKR, preferring ipsiversive stimuli. Forty-one cells had well-modulated activity and were suitable for the regression model. In these cells, an inverse dynamics approach was applied, and the time course of the SS rate was reconstructed, with mean coefficient of determination 0.76, by a linear weighted superposition of the eye acceleration (mean coefficient, 0.056 spikes/s per deg/s(2)), velocity (5.10 spikes/s per deg/s), position (-2.40 spikes/s per deg), and constant (mean 34.3 spikes/s) terms, using a time delay (mean 11 ms) from the unit response to the eye response. The velocity and acceleration terms contributed to the increase in the reconstructed SS rates during ipsilateral movements, whereas the position term contributed during contralateral movements. The standard regression coefficient analyses revealed that the contribution of the velocity term (mean coefficient 0.81) was predominant over the acceleration (0.03) and position (-0.17) terms. Forward selection analysis revealed three cell types: Velocity-Position-Acceleration type (n = 27): velocity, position, and acceleration terms are significant (P < 0.05); Velocity-Position type (n = 12): velocity and position terms are significant; and Velocity-Acceleration type (n = 2): velocity and acceleration terms are significant. Using the set of coefficients obtained by regression of the response to a 5 deg/s stimulus velocity, the SS rates during higher (10, 20, and 40 deg/s) stimulus velocities were successfully reconstructed, suggesting generality of the model. The eye-position information encoded in the SS firing during the OKR was relative but not absolute in the sense that the magnitude of the position shift from the initial eye position (0 deg/s velocity) contributed to firing rate changes, but the initial eye position did not. It is concluded that 1) the SS firing frequency in the cat middle zone encodes the velocity and acceleration information for counteracting the viscosity and inertia forces respectively, during short-duration horizontal OKR and 2) the apparent position information encoded in the SS firing is not appropriate for counteracting the elastic force during the OKR.     

Habituation of the vestibulo-ocular reflex (VOR) in the monkey during sinusoidal rotation in the dark

Summary In experimentally naive monkeys the horizontal vestibulo-ocular-reflex (VOR) has a time constant which is in the range of 40–60 s. It can be measured as the nystagmus decline after pulses of angular acceleration, or from the transfer functions obtained from sinusoidal rotation with different frequencies. When frequencies below 0.1 Hz are applied, sinusoidal rotation leads to a pronounced phase advance, a decrease in gain and a shortening of the pre- and post-rotatory nystagmus time constant. Even very low frequencies (e.g., 0.002 Hz) are effective where the phase advance of eye relative to head velocity is already 90 ° in the naive animal. Exposing the animal to stimulation only at a single frequency shifts the whole frequency curve towards a greater phase advance. These results are consistent with habituation experiments in which steps of angular velocity have repeatedly been applied. In these experiments nystagmus duration is shortened, whereas the initial response at the end of acceleration does not change. This corresponds to a phase shift and a gain reduction in the low frequency range (below 0.1 Hz) which we have also observed during sinusoidal rotation.Supported by a grant from the Swiss National Foundation for Scientific Research 3.343-0.78     

Topographical representation of vestibulo-ocular reflexes in rabbit cerebellar flocculus

In anaesthetized albino rabbits, the cerebellar flocculus was systematically mapped with a glass microelectrode to identify the location of Purkinje cells that inhibit specific vestibulo-ocular reflex pathways. The effects of microstimulation of the flocculus Purkinje cell layer on vestibular nerve-evoked reflexes to ipsilateral medial rectus, ipsilateral superior rectus and contralateral inferior oblique muscles were explored by recording electromyographically. Visual climbing fibre inputs to the flocculus were also studied by mapping field potentials evoked from both retinae.The results suggest that there are microzones in the flocculus that are related specifically to these three vestibulo-ocular reflex pathways and to different visual climbing fibre pathways.     

Motor dynamics encoding in the rostral zone of the cat cerebellar flocculus during vertical optokinetic eye movements

The complex spike (CS) and simple spike (SS) activities of Purkinje cells in the rostral zone of the cerebellar flocculus were recorded in alert cats during optokinetic responses (OKR) elicited by a stimulus sequence consisting of a constant-speed visual pattern movement in one direction for 1 s and then in the opposite direction for 1 s. The quick-phase-free trials were selected. Ninety-eight cells were identified as rostral zone cells by the direction-selective CS activity that was modulated during vertical but not horizontal stimuli. In most of the majority population (88 cells), with an increasing CS firing rate during upward OKR and an increasing SS rate during downward OKR, the inverse dynamics approach was successful and the time course of the SS rate was reconstructed (mean coefficient of determination, 0.70 and 0.72 during upward and downward stimuli, respectively) by a linear weighted superposition of the eye acceleration, velocity, position, and constant terms, at a given time delay (mean 10 ms) from the unit response to the eye-movement response. Standard regression coefficient (SRC) analysis revealed that the contribution of the velocity term (mean SRC 0.98 for upward and 0.80 for downward) to regression was dominant over acceleration (mean SRC 0.018 and 0.058) and position (-0.14 and -0.12) terms. The velocity coefficient during upward stimuli (6.6 spikes/s per degree/s) was significantly (P<0.01) larger than that during downward stimuli (4.9 spikes/s per degree/s). In most of the minority population (10 cells), with both CS and SS firing rates increasing during upward OKR, the inverse dynamics approach was not successful. It is concluded that 1) in the cat rostral zone Purkinje cells, in which the preferred direction is upward for CS and downward for SS, eye velocity and acceleration information is encoded in SS firing to counteract the viscosity and inertia forces, respectively, on the eye during vertical OKR; 2) the eye position information encoded in SS firing is inappropriate for counteracting the elastic force; 3) encoding of eye velocity information during upward OKR is quantitatively different from that during downward OKR: SS firing modulation is larger for upward than for downward OKR of the same amplitude; and 4) encoding of motor dynamics is obscure in cells in which the preferred direction is upward for both CS and SS.     

Latency of voluntary cancellation of the human vestibulo-ocular reflex during transient yaw rotation

 The effect of peripheral nerve stimulation on voluntary rhythmic flexion-extension movements at the wrist was studied in nine normal volunteers, and the results compared with the effect of cortical stimulation on the same task. In the first part of the study, magnetic stimulation was given over the inner aspect of the right arm at levels which, at rest, resulted in a wrist flexion twitch of at least 10°. We were able to confirm that this form of (peripheral-nerve) stimulation is an effective means of phase-resetting voluntary wrist movements. In addition, and unlike magnetic stimulation applied over the contralateral motor cortex, changes in the standing torque load, against which the subjects moved, had little influence on the effectiveness of this form of stimulation. Similarly, the amplitude and direction of the averaged first post-stimulus position peak (”P1”), previously identified as important determinants of the resetting induced by a cortical stimulus, were largely independent of the loading torque. In a second part to the study, we directly compared, for a constant loading torque, the resetting induced by magnetic cortical stimulation with that following magnetic stimulation of peripheral nerves. The relationship between the amplitude of P1 and the associated resetting index was identical for both forms of stimulation. Our observations indicate that magnetic stimulation of peripheral nerves is an effective means of resetting voluntary movement. It differs from magnetic cortical stimulation in that the effects of peripheral nerve stimulation are little altered by changes in loading torque. When differences in the size of P1 are allowed for, both peripheral nerve and cortical stimulation are equally effective means of resetting voluntary rhythmical movement. Received: 16 December 1997 / Accepted: 24 August 1998     

Role of cerebellar flocculus in adaptive interaction between optokinetic eye movement response and vestibulo-ocular reflex in pigmented rabbits

Summary Sustained sinusoidal oscillation of a striped cylindrical screen around a stationary, alert pigmented rabbit with certain parameters (for 4h, 5°, 7.5°, or 10° peak-to-peak, 0.1 or 0.2 Hz) adaptively modified not only the horizontal optokinetic response (HOKR) but also the horizontal vestibulo-ocular reflex (HVOR). The major effects thus obtained during 4 h were an increase in the HOKR gain by 0.23, and that of the HVOR gain by 0.18. Bilateral destruction of floccular Purkinje cells with microinjection of kainic acid abolished these effects on both HOKR and HVOR. Single unit activities of floccular Purkinje cells were recorded from the floccular areas related to horizontal eye movements (H-zone) with local stimulus effects. Most H-zone Purkinje cells normally exhibited modulation of simple spike discharge in phase with screen velocity and out of phase with turntable velocity. Sustained screen oscillation (7.5°, 0.1 Hz) for 1 h increased the simple spike responses not only to screen but also to turntable oscillation. No such changes were observed in other floccular areas. These observations suggest that sustained optokinetic stimulations induce adaptation of HVOR through an interaction of retinal slip and head velocity signals within the flocculus or its related neuronal tissues.     

Purkinje cell activity in the middle zone of the cerebellar flocculus during optokinetic and vestibular eye movement in cats

Based on the inverse dynamics theory, a previous paper reconstructed simple-spike (SS) firing rates of Purkinje cells in the cat's flocculus middle-zone by a linear-weighted summation of eye acceleration, velocity, and position during optokinetic response (OKR). The present study investigated the SS rates during combined optokinetic and vestibular stimuli of the cells recorded in the previous paper. During the sinusoidal vestibuloocular reflex (VOR) in the light (VORL) and in the dark (VORD) the firing modulation was small. During VOR suppression (VORS) by head and visual-pattern rotation in the same direction, the modulation was deep, with the peak coinciding roughly with peak ipsiversive head velocity. During VOR enhancement (VORE), the modulation was deep, with the peak coinciding roughly with peak contraversive head velocity. If we interpret these data in relation to eye and head movements, the cells in the cat were comparable to the horizontal-gaze-velocity Purkinje cells in the monkey that encode a linear summation of eye and head velocity signals. Alternatively, if we interpret the data on the basis of the inverse dynamics theory, the SS rates during VORL, VORS, and VORE were well-fitted by the OKR components of the movements (subtraction of VORD from VORL, VORS, and VORE eye movements, respectively), but not by the whole movements, using the coefficients calculated during OKR. It is concluded that the data are interpretable by both theories when the VOR gain (eye movement/head movement) is close to 1 and the firing is dominated by eye velocity information.     

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement.

1. Extracellular recordings were obtained from 113 mossu fibers (MFs) in the flocculus of alert monkeys trained to perform a visual tracking task during sinusoidal, horizontal head rotation. The analysis of MF discharge patterns was designed to allow quantitative comparison of the discharge properties of flocculus MFs with brain stem cell populations from which the MFs might originate and with flocculus Purkinje cells (P-cells). Based on their firing patterns, MFs were divided into two classes. Vestibular MFs discharged in relation to head velocity and, in some cases, also in relation to eye movement. Eye movement MFs discharged only in relation to one or more components of eye movement. 2. Vestibular MFs were subdivided into three classes. Vestibular-only MFs (n = 15) displayed a modulation in firing rate during head rotation but exhibited no relationship to spontaneous eye movements. Vestibular-plus-saccade MFs (n = 14) displayed a modulation in firing rate during head rotation that quantitatively resembled the modulation in vestibular-only MFs. In addition, a pause in firing rate interrupted the vestibular modulation during saccades in one or more directions. Vestibular-plus-position MFs (n = 4) exhibited steady firing rates that were linearly related to horizontal eye position in the absence of vestibular stimulation. Sinusoidal head rotation evoked a modulation ofiring rate above and below the firing rate set by the eye position. 3. during sinusoidal head rotation, vestibular MF firing rate led head velocity by an average of 24 degrees. The amplitude of MF firing-rate modulation increased as a function of the frequency of head rotation and, hence, maximum head velocity. Since these characteristics are similar to those displayed by P-cells during suppression of the VOR, vestibular MFs probably transmit the head velocity component of P-cell firing rate to the flocculus. Based on evidence from other mammals and a quantitative comparison of population discharge characteristics, it is likely that vestibular MFs originate from the vestibular nerve and from cells in the medial vestibular nucleus. 4. Based on their discharge patterns, eye movement MFs were also subdivided into three classes. Burst MFs (n = 14) emitted a high-frequency burst of spikes prior to and during saccades in one or more direction, but were silent during steady fixation. Burst-tonic MFs (n = 53) emitted a burst of spikes prior to saccades in a preferred ("on") direction, ceased firing during saccades in the opposite ("off") direction, and exhibited steady firing rates that increased as steady gaze shifted in the on direction. Tonic MFs (n = 13) displayed steady firing rates that increased as the position of steady gaze shifted in the on direction, and either paused or exhibited step changes in firing rate during saccades. 5. During steady fixation, 64% of tonic and burst-tonic MFs were recruited into maintained firing within +/- 10 degrees of the primary direction of gaze...