Prefrontal neuronal assemblies temporally control fear behaviour

Cyril Dejean, Julien Courtin, Nikolaos Karalis, Fabrice Chaudun, Hélène Wurtz, Thomas C. M. Bienvenu, Cyril Herry
Nature. 2016-07-01; 535(7612): 420-424
DOI: 10.1038/nature18630

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1. Nature. 2016 Jul 21;535(7612):420-4. Epub 2016 Jul 13.

Prefrontal neuronal assemblies temporally control fear behaviour.

Dejean C, Courtin J, Karalis N, Chaudun F, Wurtz H, Bienvenu TC, Herry C.

Precise spike timing through the coordination and synchronization of neuronal
assemblies is an efficient and flexible coding mechanism for sensory and
cognitive processing. In cortical and subcortical areas, the formation of cell
assemblies critically depends on neuronal oscillations, which can precisely
control the timing of spiking activity. Whereas this form of coding has been
described for sensory processing and spatial learning, its role in encoding
emotional behaviour remains unknown. Fear behaviour relies on the activation of
distributed structures, among which the dorsal medial prefrontal cortex (dmPFC)
is known to be critical for fear memory expression. In the dmPFC, the phasic
activation of neurons to threat-predicting cues, a spike-rate coding mechanism,
correlates with conditioned fear responses and supports the discrimination
between aversive and neutral stimuli. However, this mechanism does not account
for freezing observed outside stimuli presentations, and the contribution of a
general spike-time coding mechanism for freezing in the dmPFC remains to be
established. Here we use a combination of single-unit and local field potential
recordings along with optogenetic manipulations to show that, in the dmPFC,
expression of conditioned fear is causally related to the organization of neurons
into functional assemblies. During fear behaviour, the development of 4 Hz
oscillations coincides with the activation of assemblies nested in the ascending
phase of the oscillation. The selective optogenetic inhibition of dmPFC neurons
during the ascending or descending phases of this oscillation blocks and promotes
conditioned fear responses, respectively. These results identify a novel
phase-specific coding mechanism, which dynamically regulates the development of
dmPFC assemblies to control the precise timing of fear responses.

DOI: 10.1038/nature18630
PMID: 27409809 [Indexed for MEDLINE]


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