Fastigial Oculomotor Region and the Control of Foveation During Fixation

Abstract

When primates maintain their gaze directed toward a visual target (visual fixation), their eyes display a combination of miniature fast and slow movements. An involvement of the cerebellum in visual fixation is indicated by the severe gaze instabilities observed in patients suffering from cerebellar lesions. Recent studies in non-human primates have identified a cerebellar structure, the fastigial oculomotor region (FOR), as a major cerebellar output nucleus with projections toward oculomotor regions in the brain stem. Unilateral inactivation of the FOR leads to dysmetric visually guided saccades and to an offset in gaze direction when the animal fixates a visual target. However, the nature of this fixation offset is not fully understood. In the present work, we analyze the inactivation-induced effects on fixation. A novel technique is adopted to describe the generation of saccades when a target is being fixated (fixational saccades). We show that the offset is the result of a combination of impaired saccade accuracy and an altered encoding of the foveal target position. Because they are independent, we propose that these two impairments are mediated by the different projections of the FOR to the brain stem, in particular to the deep superior colliculus and the pontomedullary reticular formation. Our study demonstrates that the oculomotor cerebellum, through the activity in the FOR, regulates both the amplitude of fixational saccades and the position toward which the eyes must be directed, suggesting an involvement in the acquisition of visual information from the fovea.

Fine-Scale Plasticity of Microscopic Saccades

“…Both target-directed microsaccades and fixational saccades are continually monitored and adjusted if the stimulus shifts systematically on the retina during the movement. Oculomotor control at this microscopic level is surprising and is not predicted by mainstream hypotheses about the roles of microsaccades to prevent image fading (Ditchburn et al, 1959; and/or to reflect shifts in covert attention (Hafed and Clark, 2002;Engbert and Kliegl, 2003). It has important implications for the understanding of both sensory processing and oculomotor control.…”

“…The results of Experiment 2, however, suggest an additional function of saccadic adaptation to ensuring precise motor control. During sustained fixation, fixational saccades occur in many directions, supposedly serving the function of maintaining the gaze close to the target (Engbert et al, 2011). Fixational saccades tend to move the preferred retinal locus of fixation as often away from the target as toward it (Nachmias, 1959;Kowler and Steinman, 1980).…”

“…Microsaccades have been commonly regarded as largely "involuntary" movements necessary for preventing neural adaptation and the perceptual fading experienced in the complete absence of retinal image motion (Ditchburn et al, 1959;. But this hypothesis has remained controversial (Collewijn and Kowler, 2008;, and an emerging body of literature indicates that microsaccades are controlled movements generated to maintain fixation or acquire visual information according to the task (Hafed et al, 2009;Ko et al, 2010;Engbert et al, 2011;Otero-Millan et al, 2013;Poletti et al, 2013b).…”

Coding of Microsaccades in Three-Dimensional Space by Premotor Saccadic Neurons

“…Previous studies suggest that the direction of microsaccades can be biased by attention but are, on average, corrective, such that the eyes remains on target (Cornsweet, 1956;Guerrasio et al, 2010;Hafed, 2011;Otero-Millan et al, 2011a). Recent single neuron and lesion experiments, coupled with computational modeling of neural activity in the superior colliculus (SC), have led to the proposal that during fixation, the instantaneous locus of activity on the rostral SC is a stochastic process with zero mean (Hafed et al, 2009).…”

Similarity of superior colliculus involvement in microsaccade and saccade generation

“…Even though neurophysiological studies of microsaccade generation (Guerrasio et al 2010;Hafed 2011;Hafed et al 2009;Van Gisbergen et al 1981) are scarce relative to studies of these movements' sensory consequences (Bair and O'Keefe 1998;Bosman et al 2009;Hafed and Krauzlis 2010;Herrington et al 2009;Kagan et al 2008;Leopold and Logothetis 1998;Martinez-Conde et al 2000;Snodderly et al 2001), the existing evidence supports the hypothesis of a common mechanism. For example, preliminary results show that brainstem omnipause neurons (OPNs) pause during microsaccades just as they do during larger saccades (Brien et al 2009;Van Gisbergen et al 1981).…”