Abstract

Understanding how information about external stimuli is transformed into behavior is one of the central goals of neuroscience. Here we characterize the information flow through a complete sensorimotor circuit: from stimulus, to sensory neurons, to interneurons, to motor neurons, to muscles, to motion. Specifically, we apply a recently developed framework for quantifying information flow to a previously published ensemble of models of salt klinotaxis in the nematode worm Caenorhabditis elegans. Despite large variations in the neural parameters of individual circuits, we found that the overall information flow architecture circuit is remarkably consistent across the ensemble. This suggests structural connectivity is not necessarily predictive of effective connectivity. It also suggests information flow analysis captures general principles of operation for the klinotaxis circuit. In addition, information flow analysis reveals several key principles underlying how the models operate: (1) Interneuron class AIY is responsible for integrating information about positive and negative changes in concentration, and exhibits a strong left/right information asymmetry. (2) Gap junctions play a crucial role in the transfer of information responsible for the information symmetry observed in interneuron class AIZ. (3) Neck motor neuron class SMB implements an information gating mechanism that underlies the circuit’s state-dependent response. (4) The neck carries more information about small changes in concentration than about large ones, and more information about positive changes in concentration than about negative ones. Thus, not all directions of movement are equally informative for the worm. Each of these findings corresponds to hypotheses that could potentially be tested in the worm. Knowing the results of these experiments would greatly refine our understanding of the neural circuit underlying klinotaxis.

Highlights

  • One of the grand challenges in neuroscience is to understand how an organism’s behavior arises from the dynamical interaction between its brain, its body and its environment

  • ASEL is only sensitive to positive values of Δc and ASER is only sensitive to negative values of Δc, their responses are otherwise identical: The rise in mutual information is sharp, and the information remains relatively stable for over half the locomotion cycle, after which there is a slow decay (ASE, red trace overlaps the blue trace Fig 2)

  • We set out to analyze how information about changes in salt concentration flows through a putative minimal circuit for C. elegans klinotaxis [40, 65]

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Summary

Introduction

One of the grand challenges in neuroscience is to understand how an organism’s behavior arises from the dynamical interaction between its brain, its body and its environment. An important component of that challenge involves characterizing the flow and transformation of information through a complete neural circuit, from environmental stimuli, through sensory. Information theory [1, 2] has become an increasingly essential tool in neuroscience, with applications ranging from studies of neural coding [3, 4] and the statistical structure of environmental stimuli [5, 6], to developing maps of functional connectivity in nervous systems [7,8,9,10,11]. There has not yet been an attempt to analyze the information flow through an entire sensorimotor circuit underlying a particular behavior. The obstacles to such an endeavor are both theoretical and experimental

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