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

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. The thalamus provides sensory input to the cortex, but many aspects of thalamocortical signaling remain unknown. Here, the authors reveal parallel non-overlapping thalamic pathways with distinct representations of tactile and decision-related information during a goal-directed sensorimotor task.

Layer, cell-type and pathway-specific thalamocortical input to mouse somatosensory cortex

Berat Semihcan Sermet

In the mouse whisker system, sensory information is relayed to the whisker somatosensory cortex by two major thalamic nuclei, the ventral posterior medial nucleus (VPM) and the posterior medial nucleus (POM). While the cortical axonal innervation pattern of these two nuclei has been studied anatomically in some detail, their synaptic input to distinct cell-types across different layers in barrel cortex is incompletely understood. I used the specificity of optogenetics to selectively stimulate axons from VPM or POM, and I measured the evoked excitatory postsynaptic potentials in vitro with whole-cell patch-clamp recordings in primary whisker somatosensory cortex (wS1). VPM or POM was infected in vivo with an adenoassociated virus (AAV) encoding the light-gated cation channel channelrhodopsin (ChR2). Synaptic input onto individual neurons of the barrel cortex was recorded in brain slices in vitro by activating the ChR2-expressing thalamic axons with blue light. I measured thalamic inputs onto excitatory and three distinct classes of GABAergic neurons, expressing Parvalbumin (PV), somatostatin (SST) or vasoactive intestinal peptide (VIP) neurons across all layers of the barrel cortex. In excitatory and PV neurons, I found that the biggest inputs appeared to largely colocalize with the anatomical innervation pattern Anatomically, VPM preferentially innervates layer4 (L4), deep L3 and the L5B/6A border, and, functionally, we found that the biggest input was observed in L4, followed by L3. Anatomically, POM innervates L5A and L1, and, functionally, I found the biggest input in L5A. SST neurons received very weak input from both thalamic nuclei. VIP neurons on the other hand received larger inputs than SST neurons, however, they were weaker than excitatory and PV neurons. POM is considered to have both first-order and higher-order properties and I, therefore, began to investigate connectivity within sub-parts of POM. Taking advantage of a recently developed anterograde transsynaptic AAV injected into somatosensory brainstem nuclei, I defined first-order and higher-order sub-nuclei of POM and investigated their functional connectivity with somatosensory cortex. Anatomically, the first-order POM preferentially innervates L4 of the secondary somatosensory cortex (wS2) and functionally, I found that neurons across many layers in wS2 received direct synaptic input from first-order POM. Higher-order POM innervates both wS2 and wS1, and I found that neurons in wS2 also receive direct synaptic input. The data suggest that first-order POM relays sensory information to wS2, apparently in a parallel signaling pathway to the classical VPM to wS1 sensory pathway. In contrast, higher order POM does not appear to receive direct sensory input from the brainstem Our results begin to provide a more complete understanding of the distribution of thalamic input to specific cell-types across the layers of the mouse somatosensory cortex

EPFL2018

Layer, cell-type and pathway-specific thalamocortical input to mouse somatosensory cortex

Berat Semihcan Sermet

EPFL2018