Overt Attention toward Appetitive Cues Enhances Their Subjective Value, Independent of Orbitofrontal Cortex Activity

Abstract

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 toward 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. Macaque monkeys viewed pavlovian conditioned appetitive cues on a visual display, while the fraction of time they spent looking toward or away from the cues was measured using an eye tracker. Also measured during cue presentation were the reward anticipation, indicated by conditioned licking responses (CRs), and single-neuron activity in OFC. In general, gaze allocation predicted subsequent licking responses: the longer the monkeys spent looking at a cue at a given time point in a trial, the more likely they were to produce an anticipatory CR later in that trial, as if the subjective value of the cue were increased. To address neural mechanisms, mediation analysis measured the extent to which the gaze–CR correlation could be statistically explained by the concurrently recorded firing of OFC neurons. The resulting mediation effects were indistinguishable from chance. Therefore, while overt attention may increase the subjective value of reward-associated cues (as revealed by anticipatory behaviors), the underlying mechanism remains unknown, as does the functional significance of gaze-driven modulation of OFC value signals.

Dissociable neuronal modules in the orbitofrontal cortex representing single and multi-attribute choice tasks

“…The representation of symbol numbers in the A:B task, occurring earlier than the encoding of value signals, aligns with the idea of bottom-up attentional signals being processed in the OFC. This interpretation is supported by previous research indicating the involvement of the OFC in processing attentional signals (McGinty, 2019; McGinty et al, 2016; Xie et al, 2018). The dissociation observed between symbol number representation in the A:B task and offer quantity representation in the X:X task further suggests that these two signals may serve different cognitive functions.…”

“…As has been discussed in detail previously (Padoa-Schioppa and Cai, 2011), such representation may not be tied to a spatial location or a motor response per se. Moreover, the fact that in the A:B task symbol number signal emerged significantly earlier than the value signals is consistent with the representation of bottom-up attentional signals in the OFC (McGinty, 2019;McGinty et al, 2016;Xie et al, 2018). Moreover, the strength of association for {Symbol #, Symbol #}(A:B)1®(A:B)2 was significantly higher than that for {Symbol #, Offer Quantity}A:B®X:X.…”

Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex

“…However, in these studies, the researchers inferred the location of attention either from reward or visual salience 11 or from gaze location 9 , 10 . Without clear behavior or neurophysiology markers of attention, these studies only provided indirect evidence for the proposed theory.…”

Bottom-up but not Top-down Attention Dominates the Value Representation in the Orbitofrontal Cortex

“…Moreover, attention, both in the overt form with gaze shifts and in the covert form without eye movements, has been shown to modulate the representation of value in the orbitofrontal cortex (OFC) (McGinty, 2019;McGinty et al, 2016;Xie et al, 2018), which is a key brain area involved in value-based decision making and adaptive behavior (Ballesta et al, 2020;Hunt et al, 2018;Murray and Rudebeck, 2018;Padoa-Schioppa and Assad, 2006;Wallis and Miller, 2003). In addition, the OFC neuronal activities encoded each choice options' value alternately, which might be related to attentional shifts (Rich and Wallis, 2016).…”