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Sensory stimulation shifts visual cortex from synchronous to asynchronous states.

Tan AY, Chen Y, Scholl B, Seidemann E, Priebe NJ - Nature (2014)

Bottom Line: To distinguish between these hypotheses, 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.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.These observations show that sensory drive can shift a common cortical circuitry from a synchronous to an asynchronous state.

View Article: PubMed Central - PubMed

Affiliation: 1] Center for Perceptual Systems, University of Texas, Austin, Texas 78712, USA [2] Department of Neuroscience, College of Natural Sciences, University of Texas, Austin, Texas 78712, USA [3].

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 proposed 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. 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. Alternatively, irregular spiking could arise from infrequent correlated input events that elicit large fluctuations in Vm (refs 5, 6). To distinguish between these hypotheses, 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, 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, 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.

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Occasional large spontaneous Vm fluctuations during fixationa–c, Vm (top), horizontal and vertical eye position (bottom) from 3 blank trials, and corresponding histograms from the period indicated by the orange line (left); traces from 3 preferred orientation trials, arrow indicates stimulus onset (right); lower and upper dashed lines respectively indicate the period of required fixation, and spike threshold; a–c are different neurons. d, Distribution across neurons of distance between mean Vm during blank trials and spike threshold (n=26). e, The population Vm distribution for blank trials is the average of each neuron’s normalized mean-subtracted distribution. f, Distribution across neurons of blank trial Vm skewness. Light and dark bars in d, f indicate simple and complex cells respectively.
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Figure 2: Occasional large spontaneous Vm fluctuations during fixationa–c, Vm (top), horizontal and vertical eye position (bottom) from 3 blank trials, and corresponding histograms from the period indicated by the orange line (left); traces from 3 preferred orientation trials, arrow indicates stimulus onset (right); lower and upper dashed lines respectively indicate the period of required fixation, and spike threshold; a–c are different neurons. d, Distribution across neurons of distance between mean Vm during blank trials and spike threshold (n=26). e, The population Vm distribution for blank trials is the average of each neuron’s normalized mean-subtracted distribution. f, Distribution across neurons of blank trial Vm skewness. Light and dark bars in d, f indicate simple and complex cells respectively.

Mentions: Comparing Vm in blank trials in which no visual stimulus was presented (Fig 2a–c, left) with suprathreshold responses evoked by preferred orientation gratings (Fig. 2a–c, right) shows that blank trial Vm was generally far from spike threshold. There were occasional large depolarizations during blank trials, which manifested in the positive skewness of Vm amplitude histograms, which had longer tails at depolarized potentials, even though traces had had spikes removed (Fig. 2a–c, left, orange histograms; see also Supplementary Section 3 and Extended Data Fig. 2). Across neurons, the median distance between blank trial Vm and spike threshold was 13.9 mV (Fig. 2d). The median skewness of 0.72 (Fig. 2e, f) differs from the near zero or negative skewness expected for a range of Gaussian input (Fig. 1a; see also Supplementary Section 3 and Extended Data Fig. 2c), but is consistent with synaptic input arising from infrequent correlated events (Fig. 1b). These data show that in the absence of visual stimulation, V1 of macaques performing a visual fixation task is not in an asynchronous high conductance state1–4.


Sensory stimulation shifts visual cortex from synchronous to asynchronous states.

Tan AY, Chen Y, Scholl B, Seidemann E, Priebe NJ - Nature (2014)

Occasional large spontaneous Vm fluctuations during fixationa–c, Vm (top), horizontal and vertical eye position (bottom) from 3 blank trials, and corresponding histograms from the period indicated by the orange line (left); traces from 3 preferred orientation trials, arrow indicates stimulus onset (right); lower and upper dashed lines respectively indicate the period of required fixation, and spike threshold; a–c are different neurons. d, Distribution across neurons of distance between mean Vm during blank trials and spike threshold (n=26). e, The population Vm distribution for blank trials is the average of each neuron’s normalized mean-subtracted distribution. f, Distribution across neurons of blank trial Vm skewness. Light and dark bars in d, f indicate simple and complex cells respectively.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4067243&req=5

Figure 2: Occasional large spontaneous Vm fluctuations during fixationa–c, Vm (top), horizontal and vertical eye position (bottom) from 3 blank trials, and corresponding histograms from the period indicated by the orange line (left); traces from 3 preferred orientation trials, arrow indicates stimulus onset (right); lower and upper dashed lines respectively indicate the period of required fixation, and spike threshold; a–c are different neurons. d, Distribution across neurons of distance between mean Vm during blank trials and spike threshold (n=26). e, The population Vm distribution for blank trials is the average of each neuron’s normalized mean-subtracted distribution. f, Distribution across neurons of blank trial Vm skewness. Light and dark bars in d, f indicate simple and complex cells respectively.
Mentions: Comparing Vm in blank trials in which no visual stimulus was presented (Fig 2a–c, left) with suprathreshold responses evoked by preferred orientation gratings (Fig. 2a–c, right) shows that blank trial Vm was generally far from spike threshold. There were occasional large depolarizations during blank trials, which manifested in the positive skewness of Vm amplitude histograms, which had longer tails at depolarized potentials, even though traces had had spikes removed (Fig. 2a–c, left, orange histograms; see also Supplementary Section 3 and Extended Data Fig. 2). Across neurons, the median distance between blank trial Vm and spike threshold was 13.9 mV (Fig. 2d). The median skewness of 0.72 (Fig. 2e, f) differs from the near zero or negative skewness expected for a range of Gaussian input (Fig. 1a; see also Supplementary Section 3 and Extended Data Fig. 2c), but is consistent with synaptic input arising from infrequent correlated events (Fig. 1b). These data show that in the absence of visual stimulation, V1 of macaques performing a visual fixation task is not in an asynchronous high conductance state1–4.

Bottom Line: To distinguish between these hypotheses, 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.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.These observations show that sensory drive can shift a common cortical circuitry from a synchronous to an asynchronous state.

View Article: PubMed Central - PubMed

Affiliation: 1] Center for Perceptual Systems, University of Texas, Austin, Texas 78712, USA [2] Department of Neuroscience, College of Natural Sciences, University of Texas, Austin, Texas 78712, USA [3].

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 proposed 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. 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. Alternatively, irregular spiking could arise from infrequent correlated input events that elicit large fluctuations in Vm (refs 5, 6). To distinguish between these hypotheses, 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, 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, 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.

Show MeSH
Related in: MedlinePlus