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Nature. 2016 Jul 21;535(7612):420-4.
Prefrontal neuronal assemblies temporally control fear behaviour.
Dejean C, Courtin J, Karalis N, Chaudun F, Wurtz H, Bienvenu TC, Herry C.

Over the past decades, numerous studies demonstrated a critical role of the medial prefrontal cortex (mPFC) in regulation emotional behaviour, in particular learned fear responses. In these studies, in which the neuronal substrates of aversive learning were investigated, encoding of fear behavior was assumed to rely on the activity of single neurons through a rate coding mechanism in which the sole firing rate determine the behavioral output. This form of neuronal cording is strongly limited by the fact that over long distances, rate codes are not optimal for the fast information transmission that is required for rapid behavioural adaptation when facing threatening stimuli. In addition to this rate coding mechanism, neurons with different and specific firing sequences may cooperate and collectively provide information, a phenomenon referred to as "temporal coding".

In temporal coding, precise timing of firing is important, whereas average firing rates can remain stable. Assemblies of neurons enable temporal coding, and one of its obvious advantages is its great flexibility. Thus, neurons might rapidly switch between multiple functional networks according to sensory and internal inputs and determine specific behavioral outputs. Brain oscillations are thought to be instrumental in temporal coding by binding cell assemblies, organizing individual firing into meaningful collective activity, and coordinating remote areas. Whereas temporal coding has been described for sensory processing and spatial learning, its role in encoding emotional behaviour is virtually unknown.

To address this question 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.