Fastigial nucleus activity during different frequencies and orientations of vertical vestibular stimulation in the monkey.

Neurons in the rostral part of the fastigial nucleus (FN) respond to vestibular stimulation but are not related to eye movements. To understand the precise role of these vestibular-only neurons in the central processing of vestibular signals, unit activity in the FN of alert monkeys (Macaca mulatta) was recorded. To induce vestibular stimulation, the monkey was rotated sinusoidally around an earth-fixed horizontal axis at stimulus frequencies between 0.06 (+/-15 degrees) and 1.4 Hz (+/-7.5 degrees). During stimulation head orientation was changed continuously, allowing for roll, pitch, and intermediate planes of orientation. At a frequency of 0.6 Hz, 59% of the neurons had an optimal response orientation (ORO) and a null response (i.e., no modulation) 90 degrees apart. The phase of neuronal response was constant except for a steep shift of 180 degrees around the null response. This group I response is compatible with a semicircular canal input, canal convergence, or a single otolith input. Several other features indicated more complex responses, including spatiotemporal convergence (STC). 1) For 35% of the responses at 0.6 Hz, phase changes were gradual with different orientations. Fifteen percent of these had a null response (group II), and 20% showed only a minimal response but no null response (group III). The remaining responses (6%), classified as group IV, were characterized by a constant sensitivity at different orientations in most instances. 2) For the vast majority of neurons, the stimulus frequency determined the response group, i.e., an individual neuron could show a group I response at one frequency and a group II (III or IV) response at another frequency. 3) ORO changed with frequency by >45 degrees for 44% of the neurons. 4) Although phase changes at different frequencies were close to head velocity (+/-45 degrees ) or head position (+/-45 degrees ) for most neurons, they exceeded 90 degrees for 29% of the neurons between 0.1 and 1.0 Hz. In most cases, this was a phase advance. The change in sensitivity with change in frequency showed a similar pattern for all neurons; the average sensitivity increased from 1.24 imp. s-1. deg-1 at 0.1 Hz to 2.97 imp. s-1. deg-1 at 1.0 Hz. These data demonstrate that only an analysis based on measurements at different frequencies and orientations reveals a number of complex features. They moreover suggest that for the vast majority of neurons several sources of canal and otolith information interact at this central stage of vestibular information processing.

[1]  E P Gardner,et al.  Single-unit responses to natural vestibular stimuli and eye movements in deep cerebellar nuclei of the alert rhesus monkey. , 1975, Journal of neurophysiology.

[2]  D. Pélisson,et al.  Contribution of the rostral fastigial nucleus to the control of orienting gaze shifts in the head-unrestrained cat. , 1998, Journal of neurophysiology.

[3]  R H Schor,et al.  Tilt responses of neurons in the caudal descending nucleus of the decerebrate cat: influence of the caudal cerebellar vermis and of neck receptors. , 1996, Journal of neurophysiology.

[4]  J. Voogd Parasagittal Zones and Compartments of the Anterior Vermis of the Cat Cerebellum , 1989 .

[5]  D. Armstrong,et al.  An investigation of the cerebellar cortico-nuclear projections in the rat using an autoradiographic tracing method. I. Projections from the vermis , 1978, Brain Research.

[6]  D. Armstrong,et al.  An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. II. Projections from the hemisphere , 1978, Brain Research.

[7]  C. Batini,et al.  The GABAergic neurones of the cerebellar nuclei in the rat: Projections to the cerebellar cortex , 1989, Neuroscience Letters.

[8]  R H Schor,et al.  Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation. , 1988, Journal of neurophysiology.

[9]  B W Peterson,et al.  Sensorimotor transformation in the cat's vestibuloocular reflex system. I. Neuronal signals coding spatial coordination of compensatory eye movements. , 1993, Journal of neurophysiology.

[10]  R H Schor,et al.  Responses to head tilt in cat central vestibular neurons. II. Frequency dependence of neural response vectors. , 1985, Journal of neurophysiology.

[11]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  S. Mori,et al.  Fastigiofugal projection to the brainstem nuclei in the cat: an anterograde PHA-L tracing study , 1995, Neuroscience Research.

[13]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head movement-related activity. , 1988, Journal of neurophysiology.

[14]  U Büttner,et al.  Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. , 1997, Journal of neurophysiology.

[15]  F. Plum Handbook of Physiology. , 1960 .

[16]  H. Noda,et al.  Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey , 1990, The Journal of comparative neurology.

[17]  B. Peterson,et al.  Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats , 1984, Brain Research.

[18]  U. Büttner,et al.  A simplified calibration method for three-dimensional eye movement recordings using search-coils , 1996, Vision Research.

[19]  J. Voogd,et al.  Cerebello-vestibular connections of the anterior vermis. A retrograde tracer study in different mammals including primates. , 1991, Archives italiennes de biologie.

[20]  O. Pompeiano,et al.  Identification of cerebellar corticovestibular neurons retrogradely labeled with horseradish peroxidase , 1979, Neuroscience.

[21]  B. Peterson,et al.  Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats , 1984, Brain Research.

[22]  U Büttner,et al.  Fastigial nucleus activity in the alert monkey during slow eye and head movements. , 1991, Journal of neurophysiology.

[23]  B Cohen,et al.  Spatial Properties of Otolith Units Recorded in the Vestibular Nuclei , 1999, Annals of the New York Academy of Sciences.

[24]  S. Glasauer,et al.  Otolith Processing in the Deep Cerebellar Nuclei , 1999, Annals of the New York Academy of Sciences.

[25]  D Manzoni,et al.  Spatiotemporal response properties of cerebellar Purkinje cells to animal displacement: a population analysis , 1997, Neuroscience.

[26]  D. Snodderly,et al.  Organization of striate cortex of alert, trained monkeys (Macaca fascicularis): ongoing activity, stimulus selectivity, and widths of receptive field activating regions. , 1995, Journal of neurophysiology.

[27]  O. Pompeiano,et al.  Changes in gain and spatiotemporal properties of the vestibulospinal reflex after injection of a GABA-A agonist in the cerebellar anterior vermis. , 1997, Journal of vestibular research : equilibrium & orientation.

[28]  M. Taussig The Nervous System , 1991 .

[29]  N. Gerrits,et al.  Organization of the Vestibulocerebellum , 1996, Annals of the New York Academy of Sciences.

[30]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. , 1993, Journal of neurophysiology.