The short-term plasticity of VIP interneurons in motor cortex

Amanda R McFarlan; Isabella Gomez; Christina Y C Chou; Adam Alcolado; Rui Ponte Costa; P Jesper Sjöström

doi:10.3389/fnsyn.2024.1433977

The short-term plasticity of VIP interneurons in motor cortex

Front Synaptic Neurosci. 2024 Aug 29:16:1433977. doi: 10.3389/fnsyn.2024.1433977. eCollection 2024.

Authors

Amanda R McFarlan^{1

2}, Isabella Gomez¹, Christina Y C Chou^{1

2}, Adam Alcolado³, Rui Ponte Costa⁴, P Jesper Sjöström¹

Affiliations

¹ Centre for Research in Neuroscience, Brain Repair, and Integrative Neuroscience Program, Department of Neurology and Neurosurgery, The Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, Canada.
² Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada.
³ MTL.AI Inc., Montreal, QC, Canada.
⁴ Centre for Neural Circuits and Behaviour, Department of Physiology, Anatomy and Genetics, Medical Sciences Division, University of Oxford, Oxford, United Kingdom.

Abstract

Short-term plasticity is an important feature in the brain for shaping neural dynamics and for information processing. Short-term plasticity is known to depend on many factors including brain region, cortical layer, and cell type. Here we focus on vasoactive-intestinal peptide (VIP) interneurons (INs). VIP INs play a key disinhibitory role in cortical circuits by inhibiting other IN types, including Martinotti cells (MCs) and basket cells (BCs). Despite this prominent role, short-term plasticity at synapses to and from VIP INs is not well described. In this study, we therefore characterized the short-term plasticity at inputs and outputs of genetically targeted VIP INs in mouse motor cortex. To explore inhibitory to inhibitory (I → I) short-term plasticity at layer 2/3 (L2/3) VIP IN outputs onto L5 MCs and BCs, we relied on a combination of whole-cell recording, 2-photon microscopy, and optogenetics, which revealed that VIP IN→MC/BC synapses were consistently short-term depressing. To explore excitatory (E) → I short-term plasticity at inputs to VIP INs, we used extracellular stimulation. Surprisingly, unlike VIP IN outputs, E → VIP IN synapses exhibited heterogeneous short-term dynamics, which we attributed to the target VIP IN cell rather than the input. Computational modeling furthermore linked the diversity in short-term dynamics at VIP IN inputs to a wide variability in probability of release. Taken together, our findings highlight how short-term plasticity at VIP IN inputs and outputs is specific to synapse type. We propose that the broad diversity in short-term plasticity of VIP IN inputs forms a basis to code for a broad range of contrasting signal dynamics.

Keywords: VIP; inhibitory interneurons; motor cortex; plasticity; short-term plasticity.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. ARM was supported by doctoral awards from FRQS (287520) and HBHL. CYCC was supported by doctoral awards from NSERC CGS D 534171–2019, FRNTQ B2X 275075, HBHL, and the Ann and Richard Sievers Neuroscience Award. PJS acknowledges funding from CFI LOF 28331, CIHR PG 156223, 191969, and 191997, FRSQ CB 254033, and NSERC DG/DAS 2024–06712, 2017–04730, as well as 2017–507818. The Montreal General Hospital Foundation kindly funded the Chameleon ULTRA II laser.