Abstract

Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively.

Highlights

  • There is abundant activity in the brain in the absence of explicit sensory input or behavioral output, a phenomenon that is commonly observed in both electrophysiological and brain imaging experiments

  • Despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus

  • 15 years ago, this approach was applied in two different branches of experimental neuroscience – functional magnetic resonance imaging in humans, and electrophysiology in anesthetized cats – with results in each case demonstrating that spontaneous ongoing activity (SOA) exhibits reproducible spatiotemporal patterns that can be linked to underlying neural circuits

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Summary

Introduction

There is abundant activity in the brain in the absence of explicit sensory input or behavioral output, a phenomenon that is commonly observed in both electrophysiological and brain imaging experiments. Analyzing spontaneous neural activity poses certain experimental challenges, as there are no clearly defined task events to serve as points about which to average. 15 years ago, this approach was applied in two different branches of experimental neuroscience – functional magnetic resonance imaging (fMRI) in humans, and electrophysiology in anesthetized cats – with results in each case demonstrating that SOA exhibits reproducible spatiotemporal patterns that can be linked to underlying neural circuits. Using fMRI, Biswal et al (1995) demonstrated that spontaneous activity within a functional sensorimotor network showed strong covariation even when that network was completely at rest, a phenomenon they dubbed “functional connectivity” based largely on previous electrophysiological work (Gerstein and Perkel, 1969; Gochin et al, 1991; Friston, 1994). In the same year, Arieli et al (1995) used electrophysiological and optical techniques to show that patterns of intrinsic electrical activity in the visual cortex of anesthetized cats is coordinated at spatial scales up to several millimeters

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