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

• Published in: The European journal of neuroscience 2016-10, Vol.44 (8), p.2531-2542
• Main Authors: Sun, Zongpeng, Junker, Marc, Dicke, Peter W., Thier, Peter
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Axons - physiology; Behavior, Animal - physiology; cerebellum; Cerebellum - physiology; Eye Movements - physiology; fastigial nucleus; Macaca mulatta; microsaccades; monkey; Nerve Net - physiology; Neurons - physiology; Purkinje Cells - physiology; Saccades
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.13289

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 micro‐ and 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 microsaccade‐related 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. The cerebellar control of saccades is achieved through the fastigial oculomotor region (FOR). Lesions of the FOR compromise saccades, independent of their size, as well as fixation. Although the properties of the FOR control signals for macrosaccades are well known, it has remained unclear how the FOR contributes to the control of microsaccades and fixation. Our work shows that FOR neurons, both at an individual and population level, process control signals for saccades that are continuous across micro‐ and macrosaccades. Furthermore, by analyzing the baseline firing rate, our results suggest that FOR might play an important role in precise visual fixation.