Individual neurons in the caudal fastigial oculomotor region convey information on both macro‐ and microsaccades

Abstract

Recent studies have suggested that microsaccades, the small amplitude saccades made during fixation, are precisely controlled. Two lines of evidence suggest that the cerebellum plays a key role not only in improving the accuracy of macrosaccades but also of microsaccades. First, lesions of the fastigial oculomotor regions (FOR) cause horizontal dysmetria of both micro-and macrosaccades. Secondly, our previous work on Purkinje cell simple spikes in the oculomotor vermis (OV) has established qualitatively similar response preferences for these two groups of saccades. In this work, we investigated the control signals for microand macrosaccades in the FOR, the target of OV Purkinje cell axons. We found that the same FOR neurons discharged for micro-and macrosaccades. For both groups of saccades, FOR neurons exhibited very similar dependencies of their discharge strength on direction and amplitude and very similar burst onset time differences for ipsi-and contraversive saccades and, in both, response duration reflected saccade duration, at least at the population level. An intriguing characteristic of microsaccaderelated responses is that immediate pre-saccadic firing rates decreased with distance to the target center, a pattern that strikingly parallels the eye position dependency of both microsaccade metrics and frequency, which may suggest a potential neural mechanism underlying the role of FOR in fixation. Irrespective of this specific consideration, our study supports the view that microsaccades and macrosaccades share the same cerebellar circuitry and, in general, further strengthens the notion of a microsaccade-macrosaccade continuum.

Gaze direction as equilibrium: more evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey

“…Another explanation is physiological and lies upon the fluctuations of the activity of neurons, which, from the foveal ganglion cells to the saccade-related premotor burst neurons, exhibit sustained firing rates whenever gaze is held stable. Among this immense number of neurons, we find not only long-lead burst neurons in the pontine reticular formation, but also neurons in the caudal fastigial nucleus (Kleine et al 2003;Sun et al 2016). After unilateral inactivation of this nucleus, fixational saccades are not only dysmetric (Guerrasio et al 2010), but the direction of gaze during fixation and pursuit is also always deviated towards the lesioned side (Bourrelly et al 2018;Goffart et al 2004;Guerrasio et al 2010).…”

The Pedunculopontine Tegmental Nucleus as a Motor and Cognitive Interface between the Cerebellum and Basal Ganglia

“…On the other hand, neurons in the posterior vermis, caudal fastigial nucleus, and interpositus nucleus of the cerebellum are related to the precise and adaptive control of saccades (Robinson and Fuchs, 2001; Dash and Thier, 2014). Recent studies reported that single neurons in the oculomotor vermis and caudal fastigial nucleus discharged both for macro- and micro-saccades (Arnstein et al, 2015; Sun et al, 2016). We previously reported that neurons in the monkey PPTg showed saccade-related activity modulation, some modulations were only associated with reward-related saccades consistent with neurons reported in the basal ganglia (Kobayashi et al, 2002; Okada and Kobayashi, 2009), while others exhibited this modulation with every saccade, including small fixational saccades, consistent with neurons in the cerebellum (Okada and Kobayashi, 2014).…”

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

“…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.…”

“…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.…”

“…However, population activity on the contralateral side (left) is larger (black) than on the ipsilateral side (gray) (Herzfeld et al, 2015). Purkinje cells in OMV send inhibitory projections to the caudal fastigial nucleus (cFN), where the population response characteristics are opposite those of OMV: the response on the ipsilateral side is larger than the contralateral response (Sun et al, 2016). These neurons project to brainstem neurons, especially inhibitory burst neurons (IBNs), which, in turn, synapse on motor neurons (MNs).…”