Cerebellar output encodes a corrective saccadic command (Commentary on Sun et al.)

Abstract

The integrity of the cerebellum is critical for accurate eye movements. Disruption of neurons in either the cerebellar oculomotor vermis or its projections to the most medial output nucleus of the cerebellum, the caudal fastigial nucleus (cFN), results in significant saccadic dysmetria (Ritchie, 1976;Ohtsuka et al., 1994;Goffart et al., 2004;Buzunov et al., 2013). The relationship between cFN neuron firing rates and saccade kinematic parameters is quite variable across neurons (Hepp et al., 1982;Fuchs et al., 1993), suggesting that a direct encoding of saccade parameters may not occur in the responses of individual neurons of cFN. However, previous studies have generally agreed that saccaderelated cFN neurons tend to fire earlier for horizontal saccades made in the contraversive vs. ipsiversive directions (Ohtsuka & Noda, 1991;Fuchs et al., 1993;Helmchen & B€ uttner, 1995;Kleine et al., 2003).Taken together, these results have led to the hypothesis that saccade properties are related to the timing of responses in cFN rather than response magnitude. Under this hypothesis, neurons should fire early for contraversive saccades, helping to accelerate the eye, whereas the delayed firing of ipsiversive neurons serves to decelerate and stop the eye at saccade termination. However, new data reported by Sun et al. (2016) call this view into question.Sun and colleagues recorded single-unit cFN neuron activity while primates made saccades of various magnitudes. These saccades included very small saccades, made during periods of fixation (microsaccades), as well as larger magnitude goal-directed saccades to peripheral targets. Their results suggest that cFN neuron responses exist on a continuum between these two types of saccades. That is, micro-and macrosaccades likely share common neural mechanisms of generation. Therefore, the responses of cFN neurons can be interpreted similarly across a large range of saccadic amplitudes (e.g. 0.5-15°).The duration of a typical saccade is on the order of 60 ms. Taking advantage of the temporally short nature of saccades, Sun et al. combined the responses of individual cFN neurons recorded across different sessions to yield an estimate of the firing of a population of simultaneously recorded neurons. This population response represents an estimate of the combined response of all saccade-related cFN neurons during a saccade. Strikingly, the timing of the population response did not occur earlier for contraversive compared to ipsiversive saccades, as would be anticipated by previous single-unit studies. Rather, both directions of saccades resulted in a population response that preceded the start of the saccade, and began at approximately the same time. How can these two deep nuclei be involved in saccade acceleration and deceleration when the timing of the responses to contraversive and ipsiversive saccades are not different?We recently suggested that populations of Purkinje cells (P-cells) in the oculomotor vermis (OMV) of the cerebellum encode the velocity and direction of an impending e...

Closed-loop optogenetic perturbation of macaque oculomotor cerebellum: evidence for an internal saccade model

“…In the absence of experimental manipulation, contralateral P-cells exhibit bursts of SS activity during saccade acceleration, and they pause during saccade deceleration (Herzfeld et al, 2015, their Fig. 4, green; Herzfeld and Shadmehr, 2016). The duration of the pause may be critically important for sustaining saccade deceleration.…”

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