Top-down coordination of local cortical state during selective attention

Jochem Van Kempen,Marc A Gieselmann,Michael Boyd,Nicholas A Steinmetz,Tirin Moore,Tatiana A Engel,Alexander Thiele

doi:10.1016/j.neuron.2020.12.013

Jochem Van Kempen, Marc A Gieselmann + Show 5 more

Open Access

https://doi.org/10.1016/j.neuron.2020.12.013

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Abstract

SummarySpontaneous fluctuations in cortical excitability influence sensory processing and behavior. These fluctuations, long thought to reflect global changes in cortical state, were recently found to be modulated locally within a retinotopic map during spatially selective attention. We report that periods of vigorous (On) and faint (Off) spiking activity, the signature of cortical state fluctuations, are coordinated across brain areas with retinotopic precision. Top-down attention enhanced interareal local state coordination, traversing along the reverse cortical hierarchy. The extent of local state coordination between areas was predictive of behavioral performance. Our results show that cortical state dynamics are shared across brain regions, modulated by cognitive demands and relevant for behavior.

Highlights

Cortical activity is not solely determined by external inputs but reflects ongoing fluctuations in neural excitability referred to as cortical state (Harris and Thiele, 2011; Kohn et al, 2009)
Perception and cognition depend on the activity of many areas spanning the cortical hierarchy, which begs the question of whether cortical-state dynamics are coordinated across different brain regions during attention, whether this coordination progresses in a top-down or bottom-up manner, and whether it is relevant for behavior
Electrodes were inserted perpendicular to the cortical surface on a daily basis such that the receptive fields (RFs) overlapped both across all channels within each area and between the two areas (Figures 1B and 1C)

Summary

Introduction

Cortical activity is not solely determined by external inputs but reflects ongoing fluctuations in neural excitability referred to as cortical state (Harris and Thiele, 2011; Kohn et al, 2009). Endogenous variability in cortical state shapes sensory responses and influences behavioral performance (Arieli et al, 1996; Gutnisky et al, 2017; McGinley et al, 2015a; Renart and Machens, 2014; Scholvinck et al, 2015) These fluctuations were long thought to be a global phenomenon that influences activity throughout the cortex (Harris and Thiele, 2011; Lee and Dan, 2012), recent evidence has revealed that signatures of cortical state are modulated locally within the retinotopic map in macaque mid-level visuo-cortical area V4 during selective attention (Engel et al, 2016). Perception and cognition depend on the activity of many areas spanning the cortical hierarchy, which begs the question of whether cortical-state dynamics are coordinated across different brain regions during attention, whether this coordination progresses in a top-down or bottom-up manner, and whether it is relevant for behavior

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