Abstract

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.

Highlights

  • In natural vision, information is nearly always available at the retina

  • While it is widely acknowledged that visual activity throughout the cortical processing hierarchy depends on the interaction between stimulus qualities and properties of neurons in each cortical area, accumulating evidence suggests that during natural free viewing low frequency neuronal oscillations yoked to eye movements predictively modulate neuronal excitability in order to both amplify the neural representation of visual inputs and enhance their transmission through the visual pathways

  • This “saccadic” version of the active sensing hypothesis builds on and complements earlier formulations based on patterns of whisking and sniffing in rodents and on smaller, more rapid “fixational” eye movements in primates

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Summary

INTRODUCTION

Information is nearly always available at the retina. Yet, in primates only the central visual field has sufficient density of retinal photoreceptors to permit high-resolution vision (Curcio et al, 1990). Numerous papers have raised the logical proposition, that this active sensing regime should apply to visual sensing in primates including humans (e.g., Ahissar and Arieli, 2001, 2012; Schroeder et al, 2010), and there is evidence for this view (Purpura et al, 2003; Rajkai et al, 2008; Bartlett et al, 2011; Ito et al, 2011; Hoffman et al, 2013; Jutras et al, 2013; Hamamé et al, 2014; Staudigl et al, 2017; Katz et al, 2018; Barczak et al, 2019) Despite these wellknown attributes of natural active visual behavior, experiments designed to study visual sensory and cognitive functions usually require participants to fixate gaze at a central location while visual stimuli are presented. We outline translational implications of Active Sensing and some future directions

A ROLE FOR LOW FREQUENCY NEURAL OSCILLATIONS IN ACTIVE VISUAL SENSING
SUMMARY
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