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Distinct behavioural and network correlates of two interneuron types in prefrontal cortex

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Abstract

Neurons in the prefrontal cortex exhibit diverse behavioural correlates1,2,3,4, an observation that has been attributed to cell-type diversity. To link identified neuron types with network and behavioural functions, we recorded from the two largest genetically defined inhibitory interneuron classes, the perisomatically targeting parvalbumin (PV) and the dendritically targeting somatostatin (SOM) neurons5,6,7,8 in anterior cingulate cortex of mice performing a reward foraging task. Here we show that PV and a subtype of SOM neurons form functionally homogeneous populations showing a double dissociation between both their inhibitory effects and behavioural correlates. Out of several events pertaining to behaviour, a subtype of SOM neurons selectively responded at reward approach, whereas PV neurons responded at reward leaving and encoded preceding stay duration. These behavioural correlates of PV and SOM neurons defined a behavioural epoch and a decision variable important for foraging (whether to stay or to leave), a crucial function attributed to the anterior cingulate cortex9,10,11. Furthermore, PV neurons could fire in millisecond synchrony, exerting fast and powerful inhibition on principal cell firing, whereas the inhibitory effect of SOM neurons on firing output was weak and more variable, consistent with the idea that they respectively control the outputs of, and inputs to, principal neurons12,13,14,15,16. These results suggest a connection between the circuit-level function of different interneuron types in regulating the flow of information and the behavioural functions served by the cortical circuits. Moreover, these observations bolster the hope that functional response diversity during behaviour can in part be explained by cell-type diversity.

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Figure 1: Optogenetic tagging of genetically-defined interneurons in behaving mice.
Figure 2: Distinct inhibitory effect of SOM and PV interneurons.
Figure 3: Distinct behavioural correlates of PV and SOM interneurons.
Figure 4: PV interneurons in the ACC signal stay duration at foraging decisions.

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Acknowledgements

This work was supported by grants from the Klingenstein, John Merck, Sloan and Whitehall Foundations to A.K. and the National Institute of Neurological Disorders and Stroke (National Institutes of Health) grant R01NS075531. B.H. received support from the Swartz Foundation and Marie Curie International Outgoing Fellowship within the EU Seventh Framework Programme for Research and Technological Development (2007-2013). D.K. received support from The Robert Lee and Clara Guthrie Patterson Trust Postdoctoral Fellowship and Human Frontier Science Program (2008–2011). We are grateful to K. Deisseroth, E. Boyden, A. Reid and A. Zador for constructs, B. Burbach and R. Eifert for technical assistance, and to J. Lisman, B. Mensh, S. Shea and A. Zador for comments and discussions.

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Authors

Contributions

D.K., S.R. and A.K designed experiments. D.K. and S.R. set up and performed experiments. B.H. developed the optical tagging index. D.K., S.R., B.H. and A.K. analysed data and wrote the paper. H.T. and J.Z.H. generated SOM-Cre mice, discussed results and edited the paper.

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Correspondence to A. Kepecs.

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Kvitsiani, D., Ranade, S., Hangya, B. et al. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498, 363–366 (2013). https://doi.org/10.1038/nature12176

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