Membrane Potential Dynamics of GABAergic Neurons in the Barrel Cortex of Behaving Mice

Laboratory of Sensory Processing, Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.
Neuron (Impact Factor: 15.05). 02/2010; 65(3):422-35. DOI: 10.1016/j.neuron.2010.01.006
Source: PubMed


Computations in cortical circuits are mediated by synaptic interactions between excitatory and inhibitory neurons, and yet we know little about their activity in awake animals. Here, through single and dual whole-cell recordings combined with two-photon microscopy in the barrel cortex of behaving mice, we directly compare the synaptically driven membrane potential dynamics of inhibitory and excitatory layer 2/3 neurons. We find that inhibitory neurons depolarize synchronously with excitatory neurons, but they are much more active with differential contributions of two classes of inhibitory neurons during different brain states. Fast-spiking GABAergic neurons dominate during quiet wakefulness, but during active wakefulness Non-fast-spiking GABAergic neurons depolarize, firing action potentials at increased rates. Sparse uncorrelated action potential firing in excitatory neurons is driven by fast, large, and cell-specific depolarization. In contrast, inhibitory neurons fire correlated action potentials at much higher frequencies driven by slower, smaller, and broadly synchronized depolarization.

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Available from: Luc Gentet, Dec 28, 2015
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    • "Also, whisker-evoked responses are a product of complex interactions between cortical and subcortical brain structures, being highly dependent on stimulus timing and strength and on the state of vigilance of the animal. Thus it is conceivable that subtle alterations might not be detectable by a simple analysis of response amplitudes (Gentet et al., 2010). Furthermore we hypothesized that the increased response variance seen in the VSD recordings of whiskerevoked responses might be related to altered spontaneous cortical activity . "
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    Full-text · Article · Feb 2015 · Neurobiology of Disease
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    • "As a consequence, one predicts a smaller rise of the intraterminal basal [Ca] in in cortical excitatory terminals than measured in SL/SL Calyx terminals (Di Guilmi et al., 2014); this probably explains why the mechanism of facilitation of release (independent of Ca 2+ influx and dependent on increased basal [Ca] in ) that has been proposed to underlie the gain-of-function of AP-evoked glutamate release in Calyx (Di Guilmi et al., 2014), does not appear to contribute to the gain-of-function of excitatory transmission at SL/SL cortical pyramidal cell synapses. Nonetheless, since V resting of cortical pyramidal cells in vivo in awake animals and also in sleeping or anesthetized animals during the up-states is 10–20 mV more depolarized than that in acute cortical slices (Gentet et al., 2010; Mateo et al., 2011), the fraction of open mutant Ca V 2.1 channels and the rise of basal [Ca] in might be larger in S218L KI mice in vivo. "
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    • "Cell Reports 9, 1654–1660, December 11, 2014 ª2014 The Authors 1657 Nicotinic signaling during whisking could also contribute to the active cortical state in S1. Nonfast spiking GABAergic neocortical neurons expressing vasoactive intestinal peptide increase their activity during whisking (Gentet et al., 2010; Lee et al., 2013), in part driven by nicotinic receptor activation (Fu et al., 2014). Vasoactive intestinal peptide-expressing neurons inhibit somatostatin-expressing GABAergic neocortical neurons during whisking (Gentet et al., 2012; Lee et al., 2013; Pfeffer et al., 2013), thereby disinhibiting distal dendrites of excitatory pyramidal neurons, which are prominent locations for long-range cortical input, including excitatory projections from whisker motor cortex (M1) (Matyas et al., 2010; Petreanu et al., 2012). "
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    ABSTRACT: Internal brain states affect sensory perception, cognition, and learning. Many neocortical areas exhibit changes in the pattern and synchrony of neuronal activity during quiet versus active behaviors. Active behaviors are typically associated with desynchronized cortical dynamics. Increased thalamic firing contributes importantly to desynchronize mouse barrel cortex during active whisker sensing. However, a whisking-related cortical state change persists after thalamic inactivation, which is mediated at least in part by acetylcholine, as we show here by using whole-cell recordings, local pharmacology, axonal calcium imaging, and optogenetic stimulation. During whisking, we find prominent cholinergic signals in the barrel cortex, which suppress spontaneous cortical activity. The desynchronized state of barrel cortex during whisking is therefore driven by at least two distinct signals with opposing functions: increased thalamic activity driving glutamatergic excitation of the cortex and increased cholinergic input suppressing spontaneous cortical activity. Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved.
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