Newlands SD, Lin N, Wei M. Response linearity of alert monkey non-eye movement vestibular nucleus neurons during sinusoidal yaw rotation. J Neurophysiol 102: 1388 -1397, 2009. First published June 24, 2009 doi:10.1152/jn.90914.2008. Vestibular afferents display linear responses over a range of amplitudes and frequencies, but comparable data for central vestibular neurons are lacking. To examine the effect of stimulus frequency and magnitude on the response sensitivity and linearity of non-eye movement central vestibular neurons, we recorded from the vestibular nuclei in awake rhesus macaques during sinusoidal yaw rotation at frequencies between 0.1 and 2 Hz and between 7.5 and 210°/s peak velocity. The dynamics of the neurons' responses across frequencies, while holding peak velocity constant, was consistent with previous studies. However, as the peak velocity was varied, while holding the frequency constant, neurons demonstrated lower sensitivities with increasing peak velocity, even at the lowest peak velocities tested. With increasing peak velocity, the proportion of neurons that silenced during a portion of the response increased. However, the decrease in sensitivity of these neurons with higher peak velocities of rotation was not due to increased silencing during the inhibitory portion of the cycle. Rather the neurons displayed peak firing rates that did not increase in proportion to head velocity as the peak velocity of rotation increased. These data suggest that, unlike vestibular afferents, the central vestibular neurons without eye movement sensitivity examined in this study do not follow linear systems principles even at low velocities.
I N T R O D U C T I O NResponses of mammalian vestibular neurons, both peripheral and central, have been described for various stimulation paradigms. In vestibular afferent fibers, trade-off between the sensitivity of the cell's response and its linear range has been reported. Slow firing but sensitive irregular afferents effectively code acceleration only in the excitatory direction because once the firing rate of the neuron reaches inhibitory cutoff (rate of zero) the response of the cell remains zero (unchanged) with progressively more vigorous stimulation (Goldberg and Fernandez 1971b). Although the dynamics of vestibular afferent responses have been discussed extensively, less well understood is the impact of inhibitory cutoff and other nonlinearities in central vestibular neurons on the function of the vestibular system overall. Despite the known asymmetries in the primary afferent discharge, central mechanisms, especially the presence of a commissural system that provides informational redundancy in the vestibular nuclei, have been proposed to fill in the missing inhibitory information from one side of the midline with excitatory information from the other side (Abend 1978) to enable a linear output. Other authors have speculated on the possibilities of nonlinear processing in the central vestibular system ) and the role of population coding, which might provide...