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.
Highlights
Rodents move their whiskers to sense their nearby environment
Mechanoreceptive information from hair follicles in the whisker pad may reach these cortices via two main pathways: (a) the lemniscal pathway, that is relayed to S1BF via the ventroposterior thalamic nucleus (VPM); and (b) the paralemniscal pathway, that is relayed to both S1BF and M1wk via the posterior medial thalamic nucleus (Po; reviews in Bosman et al, 2011; Kleinfeld and Deschênes, 2011)
To gain further insight onto the neuronal circuits involved in M1wk cortex responses to passive whisker movement and their modulation by Po activation, we reduced neuronal activity in either S1BF or Po using locally applied pharmacological agents
Summary
Extracting sensory information from whisker movement crucially depends on feedback-based, precise comparisons of the intended and resulting motion. These computations are believed to be mainly carried out in the ‘‘barrel’’ field of the primary somatosensory cortex (S1BF) and the whisker region of the primary motor cortex (M1wk; Ahissar and Kleinfeld, 2003; Ferezou et al, 2007). In S1BF, VPM axons terminate mainly in layer (L), and at the edge between L5b and L6a, while Po axons target L5a and L1 (Lu and Lin, 1993; Meyer et al, 2010; Wimmer et al, 2010). In M1wk, Po axons terminate mainly in L2/3 (Deschênes et al, 1998; Ohno et al, 2012; Hooks et al, 2015)
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