Abstract

Following a stimulus, the neural response typically strongly varies in time and across neurons before settling to a steady-state. While classical population coding theory disregards the temporal dimension, recent works have argued that trajectories of transient activity can be particularly informative about stimulus identity and may form the basis of computations through dynamics. Yet the dynamical mechanisms needed to generate a population code based on transient trajectories have not been fully elucidated. Here we examine transient coding in a broad class of high-dimensional linear networks of recurrently connected units. We start by reviewing a well-known result that leads to a distinction between two classes of networks: networks in which all inputs lead to weak, decaying transients, and networks in which specific inputs elicit amplified transient responses and are mapped onto output states during the dynamics. Theses two classes are simply distinguished based on the spectrum of the symmetric part of the connectivity matrix. For the second class of networks, which is a sub-class of non-normal networks, we provide a procedure to identify transiently amplified inputs and the corresponding readouts. We first apply these results to standard randomly-connected and two-population networks. We then build minimal, low-rank networks that robustly implement trajectories mapping a specific input onto a specific orthogonal output state. Finally, we demonstrate that the capacity of the obtained networks increases proportionally with their size.

Highlights

  • The brain represents sensory stimuli in terms of the collective activity of thousands of neurons

  • Recent works have suggested that the temporal variations following the appearance and disappearance of a stimulus are strongly informative

  • We show that strong temporal variations in response to a stimulus can be generated by collective interactions within a network of neurons if the connectivity between neurons satisfies a simple mathematical criterion

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Summary

Introduction

The brain represents sensory stimuli in terms of the collective activity of thousands of neurons. As the temporal response to a stimulus is different for each neuron, an influential approach has been to represent population dynamics in terms of temporal trajectories in the neural state space, where each axis corresponds to the activity of one neuron [15,16,17,18] Coding in this high-dimensional space is typically examined by combining linear decoding and dimensionality-reduction techniques [19,20,21], and the underlying network is often conceptualised in terms of a dynamical system [18, 22,23,24,25,26,27,28,29,30]. A full theory of coding with transient trajectories is currently lacking

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