Microsaccades during fixation exhibit distinct time courses of frequency and direction modulations after stimulus onsets, but the mechanisms for these modulations are unresolved. On the one hand, microsaccade rate drops within <100 ms after stimulus onset, a phenomenon described as microsaccadic inhibition. On the other, the directions of the rare microsaccades that do occur during inhibition are, surprisingly, the most highly correlated with stimulus location. Here we show, using a combined computational and experimental approach, that these apparently dichotomous observations can simply result from a single mechanism: the phase resetting by stimulus onsets of ongoing microsaccadic oscillatory rhythms during fixation. Using experiments on monkeys and model simulations, we show that stimulus onsets act as countermanding stimuli, such as those in large saccadic countermanding tasks: they cancel an upcoming movement program and start a competing one, thus implementing phase resetting. We also show that the rare microsaccades occurring during microsaccadic inhibition are simply noncanceled movements in the countermanding framework and that they reflect the instantaneous state of visual representations expected in spatial maps representing stimuli. Remarkably, a dynamic interaction between the efficacy of the countermanding process and the metrics of the microsaccade being countermanded not only explains microsaccade rate changes, but it also predicts the time course patterns of microsaccade directions and amplitudes. Our parsimonious framework for understanding microsaccadic modulations around stimulus onsets allows analyzing microsaccades (and larger saccades) using the extensive toolkit of oscillatory dynamical systems often used for modeling spiking neurons, and it constrains neural models of microsaccade triggering.

Climbing fiber (CF) triggered complex spikes (CS) are massive depolarization bursts in the cerebellar Purkinje cell, showing several high frequency spikelet components (±600 Hz). Since its early observations, the CS is known to vary in shape. In this study we describe CS waveforms, extracellularly recorded in awake primates (Macaca mulatta) performing saccades. Every Purkinje cell analyzed showed a range of CS shapes with profoundly different duration and number of spikelets. The initial part of the CS was rather constant but the later part differed greatly, with a pronounced jitter of the last spikelets causing a large variation in total CS duration. Waveforms did not effect the following pause duration in the simple spike (SS) train, nor were SS firing rates predictive of the waveform shapes or vice versa. The waveforms did not differ between experimental conditions nor was there a preferred sequential order of CS shapes throughout the recordings. Instead, part of their variability, the timing jitter of the CS’s last spikelets, strongly correlated with interval length to the preceding CS: shorter CS intervals resulted in later appearance of the last spikelets in the CS burst, and vice versa. A similar phenomenon was observed in rat Purkinje cells recorded in vitro upon repeated extracellular stimulation of CFs at different frequencies in slice experiments. All together these results strongly suggest that the variability in the timing of the last spikelet is due to CS frequency dependent changes in Purkinje cell excitability.

Lesions of the cerebellum produce deficits in movement and motor learning. Saccadic dysmetria, for example, is caused by lesions of the posterior cerebellar vermis. Monkeys and patients with such lesions are unable to modify the amplitude of saccades. Some have suggested that the effects on eye movements might reflect a more global cognitive deficit caused by the cerebellar lesion. We tested that idea by studying the effects of vermis lesions on attention as well as saccadic eye movements, visual motion perception, and luminance change detection. Lesions in posterior vermis of four monkeys caused the known deficits in saccadic control. Attention tested by examination of acuity threshold changes induced by prior cueing of the location of the targets remained normal after vermis lesions. Luminance change detection was also unaffected by the lesions. In one case, after a lesion restricted to lobulus VIII, the animal had impaired visual motion perception.