Neocortical activity is stimulus- and scale-invariant.

Yahya Karimipanah,Rafael Yuste,Jae-eun Kang Miller,Ralf Wessel,Zhengyu Ma,Michal Zochowski

doi:10.1371/journal.pone.0177396

Yahya Karimipanah, Rafael Yuste + Show 4 more

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https://doi.org/10.1371/journal.pone.0177396

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Abstract

Mounting evidence supports the hypothesis that the cortex operates near a critical state, defined as the transition point between order (large-scale activity) and disorder (small-scale activity). This criticality is manifested by power law distribution of the size and duration of spontaneous cascades of activity, which are referred as neuronal avalanches. The existence of such neuronal avalanches has been confirmed by several studies both in vitro and in vivo, among different species and across multiple spatial scales. However, despite the prevalence of scale free activity, still very little is known concerning whether and how the scale-free nature of cortical activity is altered during external stimulation. To address this question, we performed in vivo two-photon population calcium imaging of layer 2/3 neurons in primary visual cortex of behaving mice during visual stimulation and conducted statistical analyses on the inferred spike trains. Our investigation for each mouse and condition revealed power law distributed neuronal avalanches, and irregular spiking individual neurons. Importantly, both the avalanche and the spike train properties remained largely unchanged for different stimuli, while the cross-correlation structure varied with stimuli. Our results establish that microcircuits in the visual cortex operate near the critical regime, while rearranging functional connectivity in response to varying sensory inputs.

Highlights

How does the activity of individual neurons and neuronal circuits give rise to knowledge representation, computation, and cognition? This fundamental question in neuroscience [1] is deeply confounded by the recurrent nature of cortical circuits [2,3] (Fig 1A), which shows its dynamic face (Fig 1B) in intrinsically generated cortical activity [4,5,6]
To record neuronal population spiking at cellular resolution within cortical microcircuits, we performed two-photon population calcium imaging of layer 2/3 neurons in primary visual cortex of head-fixed awake and behaving mice during three conditions of visual stimulation: dark screen, moving grating, and naturalistic movie (Fig 2A)
The testimony shown here (Figs 3 and 4) transcends beyond the coarse spatial scale of previous tests of criticality in cerebral cortex of awake subjects, which employed recordings of ongoing integrated large-scale neural activity [42,43,44,45]. Building on these important studies of macroscopic cortical activity in brain volumes consisting of thousands to millions of neurons, our results demonstrate that the principle of self-organized criticality applies down to the cellular resolution of some hundred neurons within a microcircuit embedded in the mouse visual cortex

Summary

Introduction

How does the activity of individual neurons and neuronal circuits give rise to knowledge representation, computation, and cognition? This fundamental question in neuroscience [1] is deeply confounded by the recurrent nature of cortical circuits [2,3] (Fig 1A), which shows its dynamic face (Fig 1B) in intrinsically generated cortical activity [4,5,6]. It has long been argued that recurrent cortical circuits self-organize towards a dynamical critical regime [7]. Such critical network state straddles the boundary between two distinct regimes of order and disorder [8]. The hypothesized critical dynamics, at the boundary between the two regimes, is predicted to reveal itself in the scale-free neuronal activity [9] (Fig 1C) and in the irregular nature of neuronal spiking [10] (Fig 1D). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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