Abstract

The hypothesis that brain organization is based on mechanisms of metastable synchronization in neural assemblies has been popularized during the last decades of neuroscientific research. Nevertheless, the role of body and environment for understanding the functioning of metastable assemblies is frequently dismissed. The main goal of this paper is to investigate the contribution of sensorimotor coupling to neural and behavioral metastability using a minimal computational model of plastic neural ensembles embedded in a robotic agent in a behavioral preference task. Our hypothesis is that, under some conditions, the metastability of the system is not restricted to the brain but extends to the system composed by the interaction of brain, body and environment. We test this idea, comparing an agent in continuous interaction with its environment in a task demanding behavioral flexibility with an equivalent model from the point of view of “internalist neuroscience.” A statistical characterization of our model and tools from information theory allow us to show how (1) the bidirectional coupling between agent and environment brings the system closer to a regime of criticality and triggers the emergence of additional metastable states which are not found in the brain in isolation but extended to the whole system of sensorimotor interaction, (2) the synaptic plasticity of the agent is fundamental to sustain open structures in the neural controller of the agent flexibly engaging and disengaging different behavioral patterns that sustain sensorimotor metastable states, and (3) these extended metastable states emerge when the agent generates an asymmetrical circular loop of causal interaction with its environment, in which the agent responds to variability of the environment at fast timescales while acting over the environment at slow timescales, suggesting the constitution of the agent as an autonomous entity actively modulating its sensorimotor coupling with the world. We conclude with a reflection about how our results contribute in a more general way to current progress in neuroscientific research.

Highlights

  • Neurodynamic approaches have focused in understanding what kind of neural organization is necessary to cope with the requirements of an external world

  • Our goal is to explore the relation between metastability in brain dynamics and behavior in a robotic model in order to test the hypothesis that some behavioral metastable states cannot be reduced to brain dynamics alone and are instead the product of an integration of brain, bodily and environmental dynamics

  • In this paper we have presented a neurodynamical model of oscillatory activity with synaptic activity embedded in a robotic agent in a behavioral preference task

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Summary

Introduction

Neurodynamic approaches have focused in understanding what kind of neural organization is necessary to cope with the requirements of an external world. Assuming that the brain is subject to demanding conditions from its environment, the challenge is to explain what type of neural computation or what form of organization of neural spatiotemporal patterns might be capable of satisfying the requirements for adaptive, conscious, cognitive activity. This has led to progress in the definition of a framework able to account for the brain’s ability to display a rich set of meaningful behaviors. The notion of metastable neural assemblies as building blocks of brain organization has become relatively widespread in large-scale neuroscience studies (e.g., Werner, 2007a; Buzsáki, 2010; Edelman et al, 2011; Ward, 2011)

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