A common neural mechanism mediates microsaccades and covert spatial attention

Microsaccades are small (<1°) fixational eye movements. Spatial biases in microsaccade direction reflect the focus of covert attentional selection [1]. Yet, whether microsaccades and covert attention are mediated by shared, or distinct, neural mechanisms remains actively debated [2-4]. For example, a recent study suggested that attentional modulations of neural activity in visual area V4 occur only when accompanied by microsaccades [2]. Yet, other studies have shown that behavioral and neural effects of attention occur regardless of microsaccades [3-4]. Here, we present novel evidence that reconciles these disparate findings and demonstrates a compelling mechanistic link between microsaccades and lateralized alpha-band (8-12 Hz) synchronization, a widely reported signature of functional inhibition during attention [5].
We analyzed microsaccades and scalp electroencephalography (EEG) data from n=23 participants performing a visual working memory task (1200 trials each) [4]. We observed a consistent increase in alpha-band synchronization (phase-locking value / PLV) [5], from ~200 ms preceding each microsaccade and lasting well (>300 ms) afterwards (Fig. 1D-E). Surprisingly, this increase was substantially more pronounced over the hemisphere ipsilateral, rather than contralateral, to the microsaccade (p<0.001, permutation test). Demonstrating the robustness of this association, we replicated this finding in two independently acquired datasets comprising n=38 participants performing spatial attention tasks (Fig. 1F-G).
We synthesized these findings in a computational model of the superior colliculus (SC), a midbrain structure implicated in eye-movements and attention [6] (Fig. 2). We modeled the lateralized increase in alpha-band PLV via a local inhibitory mechanism that drives microsaccades ipsilaterally through a threshold-mediated disinhibitory motif (Fig. 2A-B). Model simulations readily reconciled puzzling disconnects between microsaccades and attention-related modulations of both behavior and SC neural activity, reported recently [3]. In sum, alpha-band synchronization may represent a common neural mechanism that mediates both microsaccades and attention, motivating the need for detailed characterization of the underlying neural circuitry.