Microsaccade Control Signals in the Cerebellum

Abstract

Microsaccades, the small saccades made when we try to keep the eyes still, were once believed to be inconsequential for vision, but recent studies suggest that they can precisely relocate gaze to tiny visual targets. Because the cerebellum is necessary for motor precision, we investigated whether microsaccades may exploit this neural machinery in monkeys. Almost all vermal Purkinje cells, which provide the eye-related output of the cerebellar cortex, were found to increase or decrease their simple spike firing rate during microsaccades. At both the single-cell and population level, microsaccade-related activity was highly similar to macrosaccade-related activity and we observed a continuous representation of saccade amplitude that spanned both the macrosaccade and microsaccade domains. Our results suggest that the cerebellum's role in fine-tuning eye movements extends even to the oculomotor system's smallest saccades and add to a growing list of observations that call into question the classical categorical distinction between microsaccades and macrosaccades.

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).…”

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

“…Surgeries were carried out under combination anesthesia with remifentanil and isoflurane under aseptic conditions (see Arnstein et al . () for details). Post‐operative analgesia was continued until full recovery.…”

“…The motivation to work on the fixation and saccade task was promoted by restricting fluid provisions outside the experiment (see Arnstein et al . () for details on the protocol).…”

“…We sampled the eye movement records at a rate of 1000 Hz. Microsaccades were detected in a similar way as described before (Arnstein et al ., ): First, the eye trace was smoothed using a Savitzky‐Golay filter (second order with 20 ms width) and then eye velocity was derived from the eye position records. We employed a velocity threshold (7°/s) to identify saccades.…”

“…Arguably, the requirements for the precise control of microsaccades are even higher than for macrosaccades, assuming that their metric should be precisely determined to shift an image feature exactly into the foveola. Two findings live up to this expectation: (i) Purkinje cells in the OV are tuned for both macro‐ and microsaccades (Arnstein et al ., ). (ii) Unilateral inactivation of the caudal fastigial nucleus, the fastigial oculomotor region (FOR), causes dysmetria not only of macro‐ but also of microsaccades (Guerrasio et al ., ).…”