Multiplexed Representation of Itch and Mechanical and Thermal Sensation in the Primary Somatosensory Cortex

J Neurosci. 2021 Dec 15;41(50):10330-10340. doi: 10.1523/JNEUROSCI.1445-21.2021. Epub 2021 Oct 29.

Abstract

The primary somatosensory cortex (S1) plays a critical role in processing multiple somatosensations, but the mechanism underlying the representation of different submodalities of somatosensation in S1 remains unclear. Using in vivo two-photon calcium imaging that simultaneously monitors hundreds of layer 2/3 pyramidal S1 neurons of awake male mice, we examined neuronal responses triggered by mechanical, thermal, or pruritic stimuli. We found that mechanical, thermal, and pruritic stimuli activated largely overlapping neuronal populations in the same somatotopic S1 subregion. Population decoding analysis revealed that the local neuronal population in S1 encoded sufficient information to distinguish different somatosensory submodalities. Although multimodal S1 neurons responding to multiple types of stimuli exhibited no spatial clustering, S1 neurons preferring mechanical and thermal stimuli tended to show local clustering. These findings demonstrated the coding scheme of different submodalities of somatosensation in S1, paving the way for a deeper understanding of the processing and integration of multimodal somatosensory information in the cortex.SIGNIFICANCE STATEMENT Cortical processing of somatosensory information is one of the most fundamental aspects in cognitive neuroscience. Previous studies mainly focused on mechanical sensory processing within the rodent whisking system, but mechanisms underlying the coding of multiple somatosensations remain largely unknown. In this study, we examined the representation of mechanical, thermal, and pruritic stimuli in S1 by in vivo two-photon calcium imaging of awake mice. We revealed a multiplexed representation for multiple somatosensory stimuli in S1 and demonstrated that the activity of a small population of S1 neurons is capable of decoding different somatosensory submodalities. Our results elucidate the coding mechanism for multiple somatosensations in S1 and provide new insights that improve the present understanding of how the brain processes multimodal sensory information.

Keywords: itch; population coding; primary somatosensory cortex; sensory submodality; somatosensation; two-photon calcium imaging.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Evoked Potentials, Somatosensory / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / physiology*
  • Pruritus / physiopathology*
  • Somatosensory Cortex / physiopathology*