Synchronization of spiking activity in neuronal networks is a fundamental process that enables the precise transmission of information to drive behavioural responses1,2,3. In cortical areas, synchronization of principal-neuron spiking activity is an effective mechanism for information coding that is regulated by GABA (γ-aminobutyric acid)-ergic interneurons through the generation of neuronal oscillations4,5. Although neuronal synchrony has been demonstrated to be crucial for sensory, motor and cognitive processing6,7,8, it has not been investigated at the level of defined circuits involved in the control of emotional behaviour. Converging evidence indicates that fear behaviour is regulated by the dorsomedial prefrontal cortex9,10,11,12 (dmPFC). This control over fear behaviour relies on the activation of specific prefrontal projections to the basolateral complex of the amygdala (BLA), a structure that encodes associative fear memories13,14,15. However, it remains to be established how the precise temporal control of fear behaviour is achieved at the level of prefrontal circuits. Here we use single-unit recordings and optogenetic manipulations in behaving mice to show that fear expression is causally related to the phasic inhibition of prefrontal parvalbumin interneurons (PVINs). Inhibition of PVIN activity disinhibits prefrontal projection neurons and synchronizes their firing by resetting local theta oscillations, leading to fear expression. Our results identify two complementary neuronal mechanisms mediated by PVINs that precisely coordinate and enhance the neuronal activity of prefrontal projection neurons to drive fear expression.
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We thank members of the Herry laboratory, K. Benchenane and D. Dupret for comments on the manuscript, K. Deisseroth and E. Boyden for generously sharing material, J. Bacelo, S. Wolff and P. Tovote for technical and computational assistance, the Bordeaux Imaging center of the University of Bordeaux, and C. Poujol and S. Marais for technical assistance with microscopy. This work was supported by grants from the French National Research Agency (ANR-2010-BLAN-1442-01; ANR-10-EQPX-08 OPTOPATH), the European Research Council (ERC) under the European Union’s Seventh Framework Program (FP7/2007-2013)/ERC grant agreement no. 281168, a Fonds AXA pour la recherche doctoral fellowship (J.C.) and the Conseil Regional d’Aquitaine. T.C.M.B is a fellow of Ecole de l’Inserm Liliane Bettencourt-MD-PhD program, France.
Extended data figures
This file contains Supplementary Methods and a Supplementary Discussion. The Supplementary Methods contain additional information about the methodology used for in vitro electrophysiology, anatomical analyses, pharmacological inactivation, electrical extracellular stimulation, virus injection and optogenetics and field potential analyses. The Supplementary Discussion discusses the role of PV INs in aversive and appetitive behaviours and the origin and influence of the changes in neuronal activity observed in dmPFC PNs during fear behaviour.