Anatomically and functionally distinct thalamocortical inputs to primary and secondary mouse whisker somatosensory cortices

Sami El-Boustani,Tess B Oram,B Semihcan Sermet,Carl C H Petersen,Georgios Foustoukos,Ofer Yizhar

doi:10.1038/s41467-020-17087-7

Abstract

Subdivisions of mouse whisker somatosensory thalamus project to cortex in a region-specific and layer-specific manner. However, a clear anatomical dissection of these pathways and their functional properties during whisker sensation is lacking. Here, we use anterograde trans-synaptic viral vectors to identify three specific thalamic subpopulations based on their connectivity with brainstem. The principal trigeminal nucleus innervates ventral posterior medial thalamus, which conveys whisker-selective tactile information to layer 4 primary somatosensory cortex that is highly sensitive to self-initiated movements. The spinal trigeminal nucleus innervates a rostral part of the posterior medial (POm) thalamus, signaling whisker-selective sensory information, as well as decision-related information during a goal-directed behavior, to layer 4 secondary somatosensory cortex. A caudal part of the POm, which apparently does not receive brainstem input, innervates layer 1 and 5A, responding with little whisker selectivity, but showing decision-related modulation. Our results suggest the existence of complementary segregated information streams to somatosensory cortices.

Highlights

Subdivisions of mouse whisker somatosensory thalamus project to cortex in a region-specific and layer-specific manner
A second associated viral (AAV) injection of a Cre-dependent fluorescent protein construct in the thalamus revealed a population of neurons within the ventral posterior medial (VPM) nucleus projecting to the whisker primary somatosensory cortex (Fig. 1a), as expected for the wellcharacterized lemniscal sensory pathway[1]
Further analysis showed that the two main trigemino-thalamo-cortical circuits going through VPM and posterior medial (POm) —defined here as first-order (FO) nuclei—mainly target layer 4 (L4) of the cortex whereas the higher-order (HO) subdivision of POm targets layer 5A (L5A) and layer 1 (L1) (Fig. 1d, e)

Summary

Introduction

Subdivisions of mouse whisker somatosensory thalamus project to cortex in a region-specific and layer-specific manner. The principal trigeminal nucleus innervates ventral posterior medial thalamus, which conveys whisker-selective tactile information to layer 4 primary somatosensory cortex that is highly sensitive to self-initiated movements. The spinal trigeminal nucleus innervates a rostral part of the posterior medial (POm) thalamus, signaling whisker-selective sensory information, as well as decision-related information during a goaldirected behavior, to layer 4 secondary somatosensory cortex. It has long been hypothesized that these pathways convey distinct tactile information to the cortex in awake behaving animals Description of these thalamic networks has been challenging due to the sensitivity of their activity to brain state and their apparent heterogeneity. By using a novel adeno-associated viral (AAV) vector-based circuit mapping approach[21], we undertook to dissect thalamic circuits responsible for conveying tactile information to the cortex and probe the activity of these thalamocortical pathways in awake behaving mice. We report three distinct thalamocortical pathways to mouse whisker primary and secondary somatosensory cortices, each carrying different sensorimotor signals

Methods

Results

Conclusion