Sensory stimulation shifts visual cortex from synchronous to asynchronous states

Abstract

In the mammalian cerebral cortex, neural responses are highly variable during spontaneous activity and sensory stimulation. To explain this variability, the cortex of alert animals has been hypothesized to be in an asynchronous high conductance state in which irregular spiking arises from the convergence of large numbers of uncorrelated excitatory and inhibitory inputs onto individual neurons [1][2][3][4] . Signatures of this state are that a neuron's membrane potential (Vm) hovers just below spike threshold, and its aggregate synaptic input is nearly Gaussian, arising from many uncorrelated inputs [1][2][3][4] . Alternatively, irregular spiking could arise from infrequent correlated input events that elicit large Vm fluctuations 5,6 . To distinguish these hypotheses, we developed a technique to carry out whole-cell Vm measurements from the cortex of behaving monkeys, focusing on primary visual cortex (V1) of monkeys performing a visual fixation task. Contrary to the predictions of an asynchronous state, mean Vm during fixation was far from threshold (14 mV) and spiking was triggered by occasional large spontaneous fluctuations. Distributions of Vm values were skewed beyond that expected for a range of Gaussian input 6,7 , but were consistent with synaptic input arising from infrequent correlated events 5,6 . Furthermore, spontaneous Vm fluctuations were correlated with the surrounding network activity, as reflected in simultaneously recorded nearby local field potential (LFP). Visual stimulation, however, led to responses more consistent with an asynchronous state: mean Vm approached threshold, fluctuations became more Gaussian, and correlations between single neurons and the surrounding network were disrupted. These observations demonstrate that sensory drive can shift a common cortical circuitry from a synchronous to an asynchronous state.Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms Correspondence to: Andrew Y. Y. Tan (atyy@alum.mit.edu) and Nicholas J. Priebe (nico@austin.utexas.edu). * These authors contributed equally to this work. † These authors contributed equally to this work. Author Contributions Competing financial interestsThe authors declare no competing financial interests. HHS Public Access Author Manuscript Author ManuscriptAuthor Manuscript Author ManuscriptCortical neurons exhibit variable activity even after efforts are taken to fix temporal variations in sensory stimuli and attentional state 8 . This ongoing activity affects stimulus encoding and synaptic plasticity 9 , but its neural basis is not well understood. One hypothesis is that the variable activity in alert animals arises from connections between numerous uncorrelated excitatory and inhibitory inputs [1][2][3][4] . Such a network is consistent with studies of neural architecture 10 , and exhibits spiking statistics similar to ...

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