Scientific Understanding of Consciousness
Sensory Stimulation Shifts Visual Cortex from Synchronous to Asynchronous
Nature 509, 226–229 (08 May 2014)
Sensory stimulation shifts visual cortex from synchronous to asynchronous states
Andrew Y. Y. Tan, et.al.
Center for Perceptual Systems, University of Texas, Austin, Texas 78712, USA
Department of Neuroscience, College of Natural Sciences, University of Texas, Austin, Texas 78712, USA
Department of Psychology, University of Texas, Austin, Texas 78712, USA
In the mammalian cerebral cortex, neural responses are highly variable during spontaneous activity and sensory stimulation. 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. We developed a technique to perform whole-cell Vm measurements from the cortex of behaving monkeys, focusing on primary visual cortex (V1) of monkeys performing a visual fixation task. Here we show that 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 but were consistent with synaptic input arising from infrequent correlated events. Furthermore, spontaneous fluctuations in Vm were correlated with the surrounding network activity, as reflected in simultaneously recorded nearby local field potential. 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 show that sensory drive can shift a common cortical circuitry from a synchronous to an asynchronous state.
Cortical neurons show variable activity even after efforts are taken to fix temporal variations in sensory stimuli and attentional state. This ongoing activity affects stimulus encoding and synaptic plasticity, 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. Such a network is consistent with studies of neural architecture, and shows spiking statistics similar to those measured in extracellular studies. Predictions of this hypothesis are that numerous uncorrelated inputs cause Vm to hover near spike threshold and to show distributions that are near Gaussian or skewed with tails at hyperpolarized potentials. In contrast, neurons may receive correlated input such that Vm lies far below threshold and shows infrequent large excursions, forming skewed distributions with tails at depolarized potentials. Measurements of Vm from awake, non-behaving cats suggest an asynchronous state, but are also consistent with correlated input. Data from behaving rodents in various attentional states have suggested different pictures, but equivocally, because of the potential contributions of uncontrolled sensory inputs and attentional states to Vm dynamics. Extracellular recordings in drowsy humans have demonstrated correlated spontaneous cortical activity, leaving open the possibility that correlations are absent during alertness. Accordingly, we performed the first whole-cell Vm measurements from the cortex of monkeys actively engaged in a visual fixation task, allowing us to examine Vm in single V1 neurons of alert primates while minimizing variability due to sensory stimuli, eye movements and attentional state.
We obtained intracellular, whole-cell, current-clamp measurements of Vm from 31 V1 neurons in three macaque monkeys while they viewed gratings of different orientations. Each trial began when a fixation spot was displayed at the centre of a monitor in front of the monkey. The monkey had to shift gaze to the fixation point and maintain tight fixation for at least 1,500 ms to receive a reward. A drifting sinusoidal grating was presented for 1,000 ms while the monkey was maintaining strict fixation.
Visual stimulation increased the power of Vm fluctuations from the trial average (that is, residuals) at high frequencies (30–50 Hz) but did not cause systematic changes at low frequencies (0.5–4 Hz) (Wilcoxon signed-rank test, P = 0.76 (0.5–4 Hz), P = 0.001 (30–50 Hz).
Theory indicates that a low thalamic spike rate destabilizes the asynchronous state towards low-frequency correlations, but higher thalamic spike rates drive the network towards an asynchronous state in which correlations weaken, as observed in our data. It is clear that external drive alters the cortical state, but internal factors are also essential. In extrastriate cortex, attention causes an increase in overall response that is also accompanied by a decline in the correlation between neurons. Explaining how these external and internal drives are synthesized will require understanding how V1 interacts with downstream areas.
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