Lateral Habenula Responses During Eye Contact in a Reward Conditioning Task.

Hyunchan Lee,Okihide Hikosaka

doi:10.3389/fnbeh.2022.815461

Hyunchan Lee, Okihide Hikosaka

Open Access

https://doi.org/10.3389/fnbeh.2022.815461

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Abstract

For many animals, social interaction may have intrinsic reward value over and above its utility as a means to the desired end. Eye contact is the starting point of interactions in many social animals, including primates, and abnormal patterns of eye contact are present in many mental disorders. Whereas abundant previous studies have shown that negative emotions such as fear strongly affect eye contact behavior, modulation of eye contact by reward has received scant attention. Here we recorded eye movement patterns and neural activity in lateral habenula while monkeys viewed faces in the context of Pavlovian and instrumental conditioning tasks. Faces associated with larger rewards spontaneously elicited longer periods of eye contact from the monkeys, even though this behavior was not required or advantaged in the task. Concurrently, lateral habenula neurons were suppressed by faces signaling high value and excited by faces signaling low value. These results suggest that the reward signaling of lateral habenula may contribute to social behavior and disorders, presumably through its connections with the basal ganglia.

Highlights

Eye contact is a key element of social interactions between conspecifics and even across species
The present study found that the activities of lateral habenula (LHb) neurons are modulated by the reward history of environmental stimuli (Figure 1C)
This relationship between reward experience and gaze duration was consistently observed in both social and non-social stimuli

Summary

Introduction

Eye contact is a key element of social interactions between conspecifics and even across species. This is especially true in primates (Mosher et al, 2011). Abnormal patterns of eye contact are a common behavioral symptom in autism spectrum disorder (Szatmari et al, 2016). There have been few studies on how eye contact behavior relates to reward and reinforcement learning. Some studies have suggested that aversive feelings such as fear and avoidance lead to gaze aversion (Schneier et al, 2011), this effect is not found in all cases (Wieser et al, 2009). Given the complexity of affiliative and antagonistic behaviors in primate societies, we hypothesized that neuronal networks comprising the reward system might regulate eye contact together

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