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Ensemble encoding of action speed by striatal fast-spiking interneurons

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Abstract

Striatal fast-spiking interneurons (FSIs) potently inhibit the output neurons of the striatum and, as such, powerfully modulate action learning. Through electrical synaptic coupling, FSIs are theorized to temporally coordinate their activity. This has important implications for their ability to temporally summate inhibition on downstream striatal projection neurons. While some in vivo single-unit electrophysiological recordings of putative FSIs support coordinated firing, others do not. Moreover, it is unclear as to what aspect of action FSIs encode. To address this, we used in vivo calcium imaging of genetically identified FSIs in freely moving mice and applied machine learning analyses to decipher the relationship between FSI activity and movement. We report that FSIs exhibit ensemble activity that encodes the speed of action sub-components, including ambulation and head movements. These results suggest FSI population dynamics fit within a Hebbian model for ensemble inhibition of striatal output guiding action.

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Authors

Contributions

BMR, MGW, RC and BNM: designed the experiments. BMR: performed in vivo calcium imaging experiments. BMR and MGW: analyzed in vivo calcium imaging data. MGW and BMR: performed and analyzed electrophysiological experiments. RC: performed machine learning and simulation analyses. BMR, MGW, MHP, RC, and BNM: wrote the manuscript.

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Correspondence to Brian N. Mathur.

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Conflict of interest

The authors declare no financial and non-financial competing interests. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This work was supported by: National Institute on Alcohol Abuse and Alcoholism grants K22AA021414, R01AA024845 (B.N.M.) and F31AA024683 (M.H.P.); National Institute of General Medical Sciences grant T32008181 (M.G.W.); National Institute of Neurological Disorders and Stroke grant T32NS063391 (M.G.W.); National Institute of Neurological Disorders and Stroke and Brain Initiative grant R01NS110421 (R.C.); and National Institute of Mental Health grant F31MH112350 (M.G.W.).

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Roberts, B.M., White, M.G., Patton, M.H. et al. Ensemble encoding of action speed by striatal fast-spiking interneurons. Brain Struct Funct 224, 2567–2576 (2019). https://doi.org/10.1007/s00429-019-01908-7

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  • DOI: https://doi.org/10.1007/s00429-019-01908-7

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