Social coordination dynamics through the looking glass: Toward explaining single subject, single trial neurobehavioral variability

Abstract

A hallmark of self-organizing brain and behavioral processes lies with the multiple routes available to achieve goal-directed behavior or a particular functional outcome. If activities of the brain such as elementary visual perception or movement already show evidence of degeneracy, the same must surely be true of a complex activity such as social behavior. The challenge undertaken here is to unfold, in single individual, trial-per-trial and dynamically across time, the transient spatiotemporal patterns of brain activity that accompany social behavior. In a task of action observation and delayed imitation by pairs of individuals taken as an exemplary case study, degeneracy is revealed when comparing neuromarkers of tasks and performance from the standpoint of inter-individual average (the gold standard), with their constitutive single-individual, single trial and dynamic instances. At each level and for all patterns (electrophysiological neuromarkers, their coupling within and between brains), this comparison reveals sizeable variability that is all too often left unexplained. That is, particular time samples, single trials and single subjects are all included in the inter-individual average. Yet, such subsamples frequently do not resemble the average “gold standard”. Instead, they show more and different structures, and they appear to cluster in several types of neurobehavioral signatures. Average representations fall short of completeness in describing only a fraction of the data -a fraction that is not necessarily the most frequent as we will show-. Thereby the process of averaging undermines an understanding of the system’s functionally-adaptive diversity. From the perspective of complexity science, we set aside the interpretation that variability arises from noise in the system and its measurement. Instead, we include all meaningful neurobehavioral variables in a common analytical space in order to shed light on the interplay between neurobehavioral factors (dispositions, priors, constraints and contexts) and goal performance. Degeneracy is essential in healthy complex systems. It allows for goals to be accomplished through substantial variations in context at multiples scales of social, behavioral and neural function. By explicitly acknowledging inter-individual variation and trial to trial variability in dynamic measures of brain activity, we aim to provide a deeper multifaceted explanation of the neural basis of social behavior.