Abstract

The ability to sense, perceive, and respond appropriately to aversive cues is critical for survival. Conversely, dysfunction in any of these pathway components can lead to heightened avoidance of neutral or rewarding cues, such as social partners. The underlying circuitry mediating both negative valence processing and social behavior is particularly sensitive to early life experience, but mechanisms linking experience to pathology remain elusive. Previous research in humans, rodents, and non-human primates has highlighted the unique neurobiology of the developing infant and the role of the caregiver in mediating the infant’s negative valence circuitry, and the importance of this early social relationship for scaffolding lasting social behavior. In this review, we summarize the current literature on the development of negative valence circuits in the infant and their social regulation by the caregiver following both typical and adversity-rearing. We focus on clinically-relevant research using infant rodents which highlights the amygdala and its interface with the mesolimbic dopamine system through innervation from the ventral tegmental area (VTA) as a locus of dysfunction following early-life adversity. We then describe how these circuits are recruited to perturb life-long social behavior following adversity and propose additional therapeutic targets in these circuits with an eye toward developing age-appropriate interventions.

Highlights

  • Social support is associated with positive health outcomes, and research has demonstrated that the presence of a social-support figure can reduce psychological and physiological responses to aversive experiences (Inagaki and Eisenberger, 2012; Hornstein and Eisenberger, 2017)

  • In order for this social support to be effective, the brain-body systems responding to aversive cues, or negative valence circuits, must be functioning appropriately

  • We focus on clinically-relevant research using infant rodents which permits circuit dissection techniques to ask, how do these systems develop normally, and how does early trauma impact their lasting function to perturb social behavior? We center our discussion on the early social niche of the altricial infant, the caregiver-infant dyad, as this relationship shows unique impacts on the development of negative valence systems

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Summary

Social Regulation of Negative Valence Systems During Development

The underlying circuitry mediating both negative valence processing and social behavior is sensitive to early life experience, but mechanisms linking experience to pathology remain elusive. Rodents, and non-human primates has highlighted the unique neurobiology of the developing infant and the role of the caregiver in mediating the infant’s negative valence circuitry, and the importance of this early social relationship for scaffolding lasting social behavior. We summarize the current literature on the development of negative valence circuits in the infant and their social regulation by the caregiver following both typical and adversityrearing. We focus on clinically-relevant research using infant rodents which highlights the amygdala and its interface with the mesolimbic dopamine system through innervation from the ventral tegmental area (VTA) as a locus of dysfunction following early-life adversity.

INTRODUCTION
NEURAL CIRCUITS SUPPORTING INFANT SOCIAL BUFFERING
EARLY LIFE ADVERSITY DEGRADES SOCIAL REGULATION OF NEGATIVE VALENCE CIRCUITS
IMPLICATIONS FOR SOCIAL BEHAVIOR
COULD SOME CHANGES TO SOCIAL BEHAVIOR BE ADAPTIVE?
REMODELING OF EXTENDED NEGATIVE VALENCE CIRCUITS
CONCLUDING REMARKS
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