On the Dissociation between Microsaccade Rate and Direction after Peripheral Cues: Microsaccadic Inhibition Revisited

Abstract

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 Ͻ100 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.

Oculomotor inhibition covaries with conscious detection

“…The superior colliculus is causally involved in generating microsaccades (Hafed et al 2009). One model for oculomotor freezing is that a sensory signal arriving in the superior colliculus suppresses ongoing activity or raises the threshold for saccade execution (Hafed and Ignashchenkova 2013;Rolfs et al 2008).…”

Neuronal Response Gain Enhancement prior to Microsaccades

“…Thus, response enhancement, an attentional signature, can also occur in tight synchrony with individual microsaccades. Starting from this hypothesis, using behavioral and computational studies, we recently found that spatial attentional performance was modulated peri-microsaccadically [19,24]; the largest attentional effects occurred when targets appeared around microsaccades, during a period in which visual perception is altered [24]. Here, we investigated possible neuronal correlates of these findings.…”

“…After fixating on a spot for 400-550 ms, the spot transiently dimmed for 50 ms, which reset microsaccadic rhythms [19] without inducing a spatial bias in microsaccades. After 110-320 ms, a vertical sine wave grating (2.22 cycles/ ) appeared for 300 ms within a neuron's response field (RF) (Figure 1A).…”

“…However, subliminal gaze shifts continuously occur [17][18][19]. Microsaccades are modulated in an automatic manner by any stimulus, whether or not attentionally relevant [19,20].…”

“…However, subliminal gaze shifts continuously occur [17][18][19]. Microsaccades are modulated in an automatic manner by any stimulus, whether or not attentionally relevant [19,20]. Moreover, these eye movements are generated using similar mechanisms to larger saccades [21,22], and they are also associated with peri-movement changes in vision, similar to those accompanying saccades [23,24].…”