The Noisy Brain in Infancy: A Neurobiological Marker of Normative Social Development

Humans display a set of perceptual biases to social stimuli that are apparent early in life and set the stage for subsequent social-cognitive development. However, the degree to which different individuals show these perceptual biases and are ultimately successful at advanced social-cognitive processes varies, and in extreme cases may be indicative of disorders like autism. Successful social functioning has strong links to health outcomes; therefore, discovering the neurobiological factors that contribute to optimal social development is an important goal of widespread multidisciplinary interest. Using an individual-differences approach, this dissertation links social-behavioral outcomes to epigenetic differences within the oxytocinergic system and complexity and variability in neural signals, or “neural noise.”

It has been hypothesized that oxytocin exerts its effects on social behavior by increasing the salience of social information. This dissertation examines a neural mechanism for this hypothesis – that oxytocin increases the salience of social information by enhancing neural noise in response to social stimuli. In addition to its traditionally understood role regulating social behavior, oxytocin also acts as a neuromodulator that balances neural inhibition and excitation and regulates the signal-to-noise ratio in the brain. Therefore, early-life differences in the oxytocinergic system may trigger variable levels of neural noise during social perception and ultimately set differential developmental trajectories.

Measures of neural noise capitalize upon the inherently fluctuating nature of the brain to quantify moment-to-moment variability and complexity in neural signals. This work has revealed that neural noise increases during development, is positively associated with behavioral performance, and presents in aberrant levels in neurodevelopmental disorders like autism.

This dissertation encompasses three studies that test the hypothesis that neural noise plays a predominant role in establishing the salience of social information early in life through a process governed by the endogenous oxytocinergic system. Study 1 identifies for the first time that brain signal entropy during social perception is associated with oxytocinergic system function and social-behavioral outcomes during the first year of life. Study 2 establishes that stimuli within the auditory domain, specifically, drive these oxytocinergic-entropy-behavior associations in infancy, and replicates work of others showing an increase in brain signal entropy cooccurs with development. Study 3 demonstrates age-related changes in brain signal entropy across modalities – adults show associations between brain signal entropy and social behavior in both the visual and auditory domains.

These neurobiological markers of normative social development may be used to identify individuals at risk for atypical development before overt clinical behaviors manifest. The results of these studies provide insight into the infant’s developing brain and identify molecular and neural signatures reflective of differential developmental trajectories that persist into adulthood.