Posterior Thalamic Nucleus Modulation of Tactile Stimuli Processing in Rat Motor and Primary Somatosensory Cortices

Abstract

Rodents move rhythmically their facial whiskers and compute differences between signals predicted and those resulting from the movement to infer information about objects near their head. These computations are carried out by a large network of forebrain structures that includes the thalamus and the primary somatosensory (S1BF) and motor (M1wk) cortices. Spatially and temporally precise mechanorreceptive whisker information reaches the S1BF cortex via the ventroposterior medial thalamic nucleus (VPM). Other whisker-related information may reach both M1wk and S1BF via the axons from the posterior thalamic nucleus (Po). However, Po axons may convey, in addition to direct sensory signals, the dynamic output of computations between whisker signals and descending motor commands. It has been proposed that this input may be relevant for adjusting cortical responses to predicted vs. unpredicted whisker signals, but the effects of Po input on M1wk and S1BF function have not been directly tested or compared in vivo. Here, using electrophysiology, optogenetics and pharmacological tools, we compared in adult rats M1wk and S1BF in vivo responses in the whisker areas of the motor and primary somatosensory cortices to passive multi-whisker deflection, their dependence on Po activity, and their changes after a brief intense activation of Po axons. We report that the latencies of the first component of tactile-evoked local field potentials in M1wk and S1BF are similar. The evoked potentials decrease markedly in M1wk, but not in S1BF, by injection in Po of the GABAA agonist muscimol. A brief high-frequency electrical stimulation of Po decreases the responsivity of M1wk and S1BF cells to subsequent whisker stimulation. This effect is prevented by the local application of omega-agatoxin, suggesting that it may in part depend on GABA release by fast-spiking parvalbumin (PV)-expressing cortical interneurons. Local optogenetic activation of Po synapses in different cortical layers also diminishes M1wk and S1BF responses. This effect is most pronounced in the superficial layers of both areas, known to be the main source and target of their reciprocal cortico-cortical connections.

Variation of connectivity across exemplar sensory and associative thalamocortical loops in the mouse

“…We however noted that MD boutons in all layers of PL and in MGB boutons in layers 1, 3, and 5 of A1 are significantly smaller, than MGB boutons in layer 4 of A1. This substantial difference in bouton size is consistent with the notion that the MGB →A1 is a driver pathway ( Casas-Torremocha et al, 2017 ; Viaene et al, 2011 ), whereas the MD →PL pathway may be better described as a modulatory one. The MGB findings are also consistent with previous studies using a comparable approach ( Viaene et al, 2011 ).…”

Functional ultrasound speckle decorrelation-based velocimetry of the brain

“…We note that in addition to the significant activation of vessels in the primary somatosensory barrel field (BF), the blood vessel flowing through the posterior complex (PO) and ventral posteromedial nucleus (VPM) of the thalamus also exhibited activation. This result agrees with previous rodent functional studies that mechanoreceptive whisker information reaches the barrel cortex via the thalamic VPM nuclei 23 and the PO is a paralemniscal pathway for whisker signal processing 24 . The velocity time courses and averaged velocity relative change of the 10 trials of vessels V1 and V2 indicate robust blood flow velocity increase in response to the stimulation as shown in Figs.…”

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

“…The VPM-FO and POm-FO pathways also differ in their sensory representation during goal-directed behaviors with the former responding more strongly to self-initiated movements and the latter responding preferably to externally triggered unpredictable whisker movements 49,50 . Distinct sensory representations of self-initiated and external sensory information in parallel thalamocortical circuits have also been reported in the mouse visual system 51 and could be a general feature of sensory systems.…”