Fastigial Nucleus Activity During Different Frequencies and Orientations of Vertical Vestibular Stimulation in the Monkey

Abstract

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.

Responses of Monkey Vestibular-Only Neurons to Translation and Angular Rotation

“…Forty-two percent of the cells also responded to angular rotation about an earth-vertical axis (n ϭ 65). Similar patterns of angular and linear convergence have been reported previously in cat vestibular nucleus (Baker et al 1984;Iwamoto et al 1996;Kasper et al 1988), rat vestibular nucleus , monkey vestibular nucleus (Chen-Huang and McCrea 1999;Dickman and Angelaki 2002;Tomlinson et al 1996), and monkey fastigial nucleus (Büttner et al 1999;Shaikh et al 2005a;Siebold et al 1997Siebold et al , 1999Zhou et al 2001). …”

Vestibular Signals in Primate Thalamus: Properties and Origins

“…Cerebellothalamic pathways for vestibular signal transmission to the cortex have not been specifically described. Nevertheless, neurons in the fastigial and anterior interposed nuclei exhibit strong vestibular modulation (Gardner and Fuchs, 1975;Büttner et al, 1991;Siebold et al, 1997Siebold et al, , 1999Zhou et al, 2001;Angelaki et al, 2004;Shaikh et al, 2004Shaikh et al, , 2005a. Furthermore, thalamic projections from these nuclei primarily terminate in VL (Fig.…”

Multiple Reference Frames for Motion in the Primate Cerebellum

“…In contrast, the rostral division is populated by neurons that are modulated by vestibular stimulation but do not show sensitivity to eye movements (Gardner and Fuchs, 1975;Buttner et al, 1991;Siebold et al, 1997). Previous studies established that rostral FN neurons respond to sinusoidal rotation in horizontal and vertical planes (Gardner and Fuchs, 1975;Siebold et al, 1997Siebold et al, , 1999 as well as to translational movements (Zhou et al, 2001). Given the afferent and efferent projections of rostral FN neurons, it is believed that they are involved in vestibulospinal control, including regulation of gait and postural mechanisms (Gardner and Fuchs, 1975;Buttner et al, 1991;Siebold et al, 1997).…”