Properties of Cerebellar Fastigial Neurons During Translation, Rotation, and Eye Movements (original) (raw)
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Frequency-Selective Coding of Translation and Tilt in Macaque Cerebellar Nodulus and Uvula
Journal of Neuroscience, 2008
Spatial orientation depends critically on the brain's ability to segregate linear acceleration signals arising from otolith afferents into estimates of self-motion and orientation relative to gravity. In the absence of visual information, this ability is known to deteriorate at low frequencies. The cerebellar nodulus/uvula (NU) has been shown to participate in this computation, although its exact role remains unclear. Here, we show that NU simple spike (SS) responses also exhibit a frequency dependent selectivity to self-motion (translation) and spatial orientation (tilt). At 0.5 Hz, Purkinje cells encode three-dimensional translation and only weakly modulate during pitch and roll tilt (0.4 Ϯ 0.05 spikes/s/°/s). But this ability to selectively signal translation over tilt is compromised at lower frequencies, such that at 0.05 Hz tilt response gains average 2.0 Ϯ 0.3 spikes/s/°/s. We show that such frequency-dependent properties are attributable to an incomplete cancellation of otolith-driven SS responses during tilt by a canal-driven signal coding angular position with a sensitivity of 3.9 Ϯ 0.3 spikes/s/°. This incomplete cancellation is brought about because otolith-driven SS responses are also partially integrated, thus encoding combinations of linear velocity and acceleration. These results are consistent with the notion that NU SS modulation represents an internal neural representation of similar frequency dependencies seen in behavior.
Spatiotemporal Properties of Optic Flow and Vestibular Tuning in the Cerebellar Nodulus and Uvula
Journal of Neuroscience, 2013
Convergence of visual motion and vestibular information is essential for accurate spatial navigation. Such multisensory integration has been shown in cortex, e.g., the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas, but not in the parieto-insular vestibular cortex (PIVC). Whether similar convergence occurs subcortically remains unknown. Many Purkinje cells in vermal lobules 10 (nodulus) and 9 (uvula) of the macaque cerebellum are tuned to vestibular translation stimuli, yet little is known about their visual motion responsiveness. Here we show the existence of translational optic flow-tuned Purkinje cells, found exclusively in the anterior part of the nodulus and ventral uvula, near the midline. Vestibular responses of Purkinje cells showed a remarkable similarity to those in MSTd (but not PIVC or VIP) neurons, in terms of both response latency and relative contributions of velocity, acceleration, and position components. In contrast, the spatiotemporal properties of optic flow responses differed from those in MSTd, and matched the vestibular properties of these neurons. Compared with MSTd, optic flow responses of Purkinje cells showed smaller velocity contributions and larger visual motion acceleration responses. The remarkable similarity between the nodulus/uvula and MSTd vestibular translation responsiveness suggests a functional coupling between the two areas for vestibular processing of self-motion information.
Pursuit--Vestibular Interactions in Brain Stem Neurons During Rotation and Translation
Journal of Neurophysiology, 2005
Under natural conditions, the vestibular and pursuit systems work synergistically to stabilize the visual scene during movement. How translational vestibular signals [translational vestibuloocular reflex (TVOR)] are processed in the premotor pathways for slow eye movements continues to remain a challenging question. To further our understanding of how premotor neurons contribute to this processing, we recorded neural activities from the prepositus and rostral medial vestibular nuclei in macaque monkeys. Vestibular neurons were tested during 0.5-Hz rotation and lateral translation (both with gaze stable and during VOR cancellation tasks), as well as during smooth pursuit eye movements. Data were collected at two different viewing distances, 80 and 20 cm. Based on their responses to rotation and pursuit, eye-movement–sensitive neurons were classified into position–vestibular–pause (PVP) neurons, eye–head (EH) neurons, and burst–tonic (BT) cells. We found that approximately half of the...
Direction Discrimination Thresholds of Vestibular and Cerebellar Nuclei Neurons
Journal of Neuroscience, 2010
McCrea, Robert A., Greg T. Gdowski, Richard Boyle, and Timothy Belton. Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J. Neurophysiol. 82: 416-428, 1999. The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n ϭ 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.
Convergence of directional vestibular and neck signals on cerebellar Purkinje cells
Pfl�gers Archiv European Journal of Physiology, 1998
Convergence of spatially oriented vestibular and neck signals within the cerebellar anterior vermis in decerebrate cats was studied by recording the simple spike discharge of Purkinje (P) cells during wobble either of the whole animal (vestibular input) or of the body under a fixed head (neck input) at 0.156 Hz, 5°a nd 2.5°, respectively. Both clockwise (CW) and counterclockwise (CCW) rotations were performed. Units that had equal response amplitudes to CW and CCW rotations (narrowly tuned neurons) were described by a single vector (S max ), characterized by a gain, a direction and a temporal phase. Units with different response amplitudes to CW and CCW rotation (broadly tuned neurons) were described by two vectors (S max and S min ). In addition to these bidirectional units, there were also unidirectional units which responded either to CW or CCW rotation; in these cases the gain of S max equals that of S min . On the whole, 77% and 63% of the P cells responding to vestibular and neck stimulation, respectively, showed a bidirectional broadly tuned or unidirectional behavior. These response patterns were attributed to the convergence of signals with different spatial and temporal properties. About 50% of the P cells from which recordings were made responded to stimulation of both sensory systems. However, the gains of the S max vectors of the neck responses were much greater than those of the vestibular responses, at least for small amplitudes of rotation, and were positively correlated with them. Usually the differences in the orientation components of the neck and vestibular S max vectors were larger, while the differences in temporal phases were smaller than 90°. These findings suggest that periodic changes in the phase difference and gain ratio of the neck to the vestibular response may occur during dynamic displacement of the head over the body, depending on the stimulus direction. As a result of these data, the P cells of the cerebellar vermis are expected to show prominent responses to head rotation, which could affect the spatially organized postural responses by utilizing vestibular and reticular targets.
Neuroscience, 1999
The activity of 68 neurons, mainly Purkinje cells, was recorded from the cerebellar anterior vermis of decerebrate cats during wobble of the whole animal (at 0.156 Hz, 5Њ), a mixture of tilt and rotation, leading to stimulation of labyrinth receptors. Most of the neurons (65/68) were affected by both clockwise and counterclockwise rotations. Twenty-four units showing responses of comparable amplitude to these stimuli (narrowly tuned cells) were represented by a single vector (S max ), whose preferred direction corresponded to the direction of stimulation giving rise to the maximal response. The remaining 41 units, however, showed different amplitude responses to these rotations (broadly tuned cells) and were characterized by two spatially and temporally orthogonal vectors (S max and S min ), suggesting that labyrinthine signals with different spatial and temporal properties converged on these cells. All these units were tested while the body was aligned with the head (control position), as well as after static displacement of the body under a fixed head by 15Њ and/or 30Њ around a vertical axis passing through C1-C2, thus leading to stimulation of neck receptors. The orientation component of the response vector of the Purkinje cells to vestibular stimulation changed following body-to-head displacement. Moreover, the amplitude of vector rotation corresponded, on the average, to that of body rotation. Changes in temporal phase, gain and tuning ratio of the responses were also observed.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2018
Many daily behaviors rely critically on estimates of our body motion. Such estimates must be computed by combining neck proprioceptive signals with vestibular signals that have been transformed from a head- to a body-centered reference frame. Recent studies showed that deep cerebellar neurons in the rostral fastigial nucleus (rFN) reflect these computations, but whether they explicitly encode estimates of body motion remains unclear. A key limitation in addressing this question is that to date cell tuning properties have only been characterized for a restricted set of motions across head-re-body orientations in the horizontal plane. Here we examined for the first time how 3D spatio-temporal tuning for translational motion varies with head-re-body orientation in both horizontal and vertical planes in the rFN of male macaques. While vestibular coding was profoundly influenced by head-re-body position in both planes, neurons typically reflected at most a partial transformation. However...
2010
Convergent properties of vestibular-related brain stem neurons in the gerbil. J. Neurophysiol. 83: 1958Neurophysiol. 83: -1971Neurophysiol. 83: , 2000. Three classes of vestibular-related neurons were found in and near the prepositus and medial vestibular nuclei of alert or decerebrate gerbils, those responding to: horizontal translational motion, horizontal head rotation, or both. Their distribution ratios were 1:2:2, respectively. Many cells responsive to translational motion exhibited spatiotemporal characteristics with both response gain and phase varying as a function of the stimulus vector angle. Rotationally sensitive neurons were distributed as Type I, II, or III responses (sensitive to ipsilateral, contralateral, or both directions, respectively) in the ratios of 4:6:1. Four tested factors shaped the response dynamics of the sampled neurons: canal-otolith convergence, oculomotor-related activity, rotational Type (I or II), and the phase of the maximum response. Type I nonconvergent cells displayed increasing gains with increasing rotational stimulus frequency (0.1-2.0 Hz, 60°/s), whereas Type II neurons with convergent inputs had response gains that markedly decreased with increasing translational stimulus frequency (0.25-2.0 Hz, Ϯ0.1 g). Type I convergent and Type II nonconvergent neurons exhibited essentially flat gains across the stimulus frequency range. Oculomotor-related activity was noted in 30% of the cells across all functional types, appearing as burst/pause discharge patterns related to the fast phase of nystagmus during head rotation. Oculomotor-related activity was correlated with enhanced dynamic range compared with the same category that had no oculomotor-related response. Finally, responses that were in-phase with head velocity during rotation exhibited greater gains with stimulus frequency increments than neurons with out-of-phase responses. In contrast, for translational motion, neurons out of phase with head acceleration exhibited low-pass characteristics, whereas in-phase neurons did not. Data from decerebrate preparations revealed that although similar response types could be detected, the sampled cells generally had lower background discharge rates, on average one-third lower response gains, and convergent properties that differed from those found in the alert animals. On the basis of the dynamic response of identified cell types, we propose a pair of models in which inhibitory input from vestibular-related neurons converges on oculomotor neurons with excitatory inputs from the vestibular nuclei. Simple signal convergence and combinations of different types of vestibular labyrinth information can enrich the dynamic characteristics of the rotational and translational vestibuloocular responses.
Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum
Journal of Neurophysiology, 2007
We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibulo-ocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, 3-D eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200 °/s 2 to 40 °/s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0°, ± 15°) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations the effect was not seen at the onset of head rotation, when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope, but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: 1) the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and 2) once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed. Angelaki DE. Three-dimensional ocular kinematics during eccentric rotations: evidence for functional rather than mechanical constraints. J Neurophysiol 89: 2685-2696, 2003. Angelaki DE and Hess BJ. Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. versus full-field visual stabilization strategies for translational and rotational head movements. J Neurosci 23: 1104-1108, 2003. Bergamin O, Ramat S, Straumann D and Zee DS. Influence of orientation of exiting wire of search coil annulus on torsion after saccades. Invest Ophthalmol Vis Sci 45: 131-137, 2004. Blazquez PM, Hirata Y, Heiney SA, Green AM and Highstein SM. Cerebellar signatures of vestibulo-ocular reflex motor learning. J Neurosci 23: 9742-9751, 2003. Crane BT, Tian J and Demer JL. Kinematics of vertical saccades during the yaw vestibulo-ocular reflex in humans.
Cerebellar Disease Alters the Axis of the High-Acceleration Vestibuloocular Reflex
Journal of Neurophysiology, 2005
Walker, Mark F. and David S. Zee. Cerebellar disease alters the axis of the high-acceleration vestibuloocular reflex. showed that the axis of the rotational vestibuloocular reflex (RVOR) cannot be altered by visual-vestibular mismatch ("crossaxis adaptation") when the vestibulocerebellum is lesioned. This suggests that the cerebellum may calibrate the axis of eye velocity of the RVOR under natural conditions. Thus we asked whether patients with cerebellar disease have alterations in the RVOR axis and, if so, what might be the mechanism. We used three-axis scleral coils to record head and eye movements during yaw, pitch, and roll head impulses in 18 patients with cerebellar disease and in a comparison group of eight subjects without neurologic disease. We found distinct shifts of the eye-velocity axis in patients. The characteristic finding was a disconjugate upward eye velocity during yaw. Measured at 70 ms after the onset of head rotation, the median upward gaze velocity was 15% of yaw head velocity for patients and Ͻ1% for normal subjects (P Ͻ 0.001). Upward eye velocity was greater in the contralateral (abducting) eye during yaw and in the ipsilateral eye during roll. Patients had a higher gain (eye speed/head speed) for downward than for upward pitch (median ratio of downward to upward gain: 1.3). In patients, upward gaze velocities during both yaw and roll correlated with the difference in anterior (AC) and posterior canal excitations, scaled by the respective pitch gains. Our findings support the hypothesis that upward eye velocity during yaw results from AC excitation, which must normally be suppressed by the intact cerebellum.