Orbitofrontal Cortex Value Signals Depend on Fixation Location during Free Viewing

Abstract

SUMMARY In the natural world, monkeys and humans judge the economic value of numerous competing stimuli by moving their gaze from one object to another, in a rapid series of eye movements. This suggests that the primate brain processes value serially, and that value-coding neurons may be modulated by changes in gaze. To test this hypothesis, we presented monkeys with value-associated visual cues, and took the unusual step of allowing unrestricted free viewing while we recorded neurons in the orbitofrontal cortex (OFC). By leveraging natural gaze patterns, we found that a large proportion of OFC cells encode gaze location, and that in some cells, value coding is amplified when subjects fixate near the cue. These findings provide the first cellular-level mechanism for previously documented behavioral effects of gaze on valuation, and suggest a major role for gaze in neural mechanisms of valuation and decision-making under ecologically realistic conditions.

A Spotlight on Reward

“…This possibility accounts for a remarkable feature of McGinty et al (2016)'s study (Figure 1, middle panel). They found classic OFC reward-related responses in the absence of any economic choice task.…”

“…Research published in this issue of Neuron from McGinty et al (2016) suggests that attention may help bind information about value to specific options in economic choice. Responses of orbitofrontal neurons are strongly modulated by the distance from gaze to the position of a reward-predicting target.…”

Overt attention towards appetitive cues enhances their subjective value, independent of orbitofrontal cortex activity

“…Several recent studies have shown that value representations in the prefrontal cortex can be influenced by how attention is allocated among visual objects of different value. This includes overt shifts of attention (gaze) performed during natural free viewing (McGinty et al, 2016;Hunt et al, 2018), as well as covert shifts of attention performed in the absence of saccadic eye movements (Xie et al, 2018).…”

“…A natural hypothesis emerging from these studies is that attention, by modulating neural value signals, may influence a wide range of value-driven behaviors. To test this hypothesis, we build upon our recent report of gazemodulated value signals in the primate orbitofrontal cortex during appetitive Pavlovian conditioning (McGinty et al, 2016). Whereas the prior report considered only the neural effects of gaze, here we address both the neural and behavioral effects, and ask whether the neural effects are sufficient to explain behavior.…”

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Neural representations of value underlie many behaviors that are crucial for survival. Previously, we found that value representations in primate orbitofrontal cortex (OFC) are modulated by attention, specifically, by overt shifts of gaze towards or away from reward-associated visual cues (McGinty et al, 2016). Here, we investigate the influence of overt attention on behavior, by asking how gaze shifts correlate with reward anticipatory responses, and whether activity in OFC mediates this correlation.

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