The Role of Neuronal Oscillations in Visual Active Sensing

Visual perception is most often studied as a "passive" process in which an observer fixates steadily at point in space so that stimuli can be delivered to the system with spatial precision. Analysis of neuronal signals related to vision is generally keyed to stimulus onset, stimulus movement, etc.; i.e., events external to the observer. In natural "active" vision, however, information is systematically acquired by using eye movements including rapid (saccadic) eye movements, as well as smooth ocular pursuit of moving objects and slower drifts. Here we consider the use of alternating saccades and fixations to gather information from a visual scene. The underlying motor sampling plan contains highly reliable information regarding "where" and "when" the eyes will land, this information can be used predictively to modify firing properties of neurons precisely at the time when this "contextual" information is most useful - when a volley of retinal input enters the system at the onset of each fixation. Analyses focusing on neural events leading to and resulting from shifts in fixation, as well as visual events external to the observer, can provide a more complete and mechanistic understanding of visual information processing. Studies thus far suggest that active vision may be a fundamentally different from that process we usually study with more traditional passive viewing paradigms. In this Perspective we note that active saccadic sampling behavior imposes robust temporal patterning on the activity of neuron ensembles and large-scale neural dynamics throughout the brain's visual pathways whose mechanistic effects on information processing are not yet fully understood. The spatio-temporal sequence of eye movements elicits a succession of temporally predictable quasi-rhythmic sensory inputs, whose encoding is enhanced by entrainment of low frequency oscillations to the rate of eye movements. Review of the pertinent findings underscores the fact that temporal coordination between motor and visual cortices is critical for understanding neural dynamics of active vision and posits that phase entrainment of neuronal oscillations plays a mechanistic role in this process.