In Vivo Optogenetic Stimulation of Neocortical Excitatory Neurons Drives Brain-State-Dependent Inhibition
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Author(s)
Mateo, Celine
Avermann, Michael
Gentet, Luc J.
Zhang, Feng
Deisseroth, Karl
Petersen, Carl C.H.
Date Issued
September 2011
Journal
Current Biology
Publisher
Elsevier
Citation
Mateo, Celine, Michael Avermann, Luc J. Gentet, Feng Zhang, Karl Deisseroth, and Carl C.H. Petersen. “In Vivo Optogenetic Stimulation of Neocortical Excitatory Neurons Drives Brain-State-Dependent Inhibition.” Current Biology 21, no. 19 (October 2011): 1593–1602. © 2011 Elsevier Ltd.
Version
Final published version
Abstract
Background
Synaptic interactions between excitatory and inhibitory neocortical neurons are important for mammalian sensory perception. Synaptic transmission between identified neurons within neocortical microcircuits has mainly been studied in brain slice preparations in vitro. Here, we investigate brain-state-dependent neocortical synaptic interactions in vivo by combining the specificity of optogenetic stimulation with the precision of whole-cell recordings from postsynaptic excitatory glutamatergic neurons and GFP-labeled inhibitory GABAergic neurons targeted through two-photon microscopy.
Results
Channelrhodopsin-2 (ChR2) stimulation of excitatory layer 2/3 barrel cortex neurons evoked larger and faster depolarizing postsynaptic potentials and more synaptically driven action potentials in fast-spiking (FS) GABAergic neurons compared to both non-fast-spiking (NFS) GABAergic neurons and postsynaptic excitatory pyramidal neurons located within the same neocortical microcircuit. The number of action potentials evoked in ChR2-expressing neurons showed low trial-to-trial variability, but postsynaptic responses varied strongly with near-linear dependence upon spontaneously driven changes in prestimulus membrane potential. Postsynaptic responses in excitatory neurons had reversal potentials, which were hyperpolarized relative to action potential threshold and were therefore inhibitory. Reversal potentials measured in postsynaptic GABAergic neurons were close to action potential threshold. Postsynaptic inhibitory neurons preferentially fired synaptically driven action potentials from spontaneously depolarized network states, with stronger state-dependent modulation in NFS GABAergic neurons compared to FS GABAergic neurons.
Conclusions
Inhibitory neurons appear to dominate neocortical microcircuit function, receiving stronger local excitatory synaptic input and firing more action potentials compared to excitatory neurons. In mouse layer 2/3 barrel cortex, we propose that strong state-dependent recruitment of inhibitory neurons drives competition among excitatory neurons enforcing sparse coding.
MIT Department
Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
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Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use.
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DOI of Published Version
https://doi.org/10.1016/j.cub.2011.08.028
