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

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 goaldirected 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.

Nonlinear collision between anisotropic propagating waves in mouse somatosensory cortex

“…As already discussed in the result section, a propagating wave originating outside S1 appears around 20 ms after whisker stimulation and propagates toward whiskers representation in S1. This wave is originating in S2 which receives direct tactile sensory inputs from the thalamus (Carvell & Simons, 1987;El-Boustani et al, 2020;Minamisawa et al, 2018), as well as a monosynaptic drive from S1 through axons travelling in deep cortical layers (Minamisawa et al, 2018). As shown in (Hubatz et al, 2020), S2 comprises a discernable topographic arrangement of individual whisker representations, and responds with a similar intensity to individual whisker stimulation as S1, but with a slight delay in time.…”

NMDA receptor–BK channel coupling regulates synaptic plasticity in the barrel cortex

“…Presynaptic electrical stimulation of basal afferent inputs was performed in the limit between layers 5 and 6. This approach has been widely described to activate an important contribution of ascending thalamocortical fibers (Manns et al, 2004;Núñez et al, 2012), many of which are known to directly connect with BC-L5PN (Agmon and Connors, 1992;Constantinople and Bruno, 2013;El-Boustani et al, 2020;Rodriguez-Moreno et al, 2020). The presence or absence of a Ca 2+ spike in the evoked action potential allowed us to classify cells as A-type or B-type BC-L5PN.…”

“…To investigate the effect of NMDAR-BK coupling on synaptic transmission, we electrically stimulated the afferent inputs to BC-L5PN basal dendrites and recorded evoked postsynaptic potentials (PSPs) in physiological conditions (with Mg 2+ in the external solution). Presynaptic stimulation of basal afferent inputs was performed at the limit between layers 5 and 6 to activate ascending thalamocortical fibers (Manns et al, 2004;Nunez et al, 2012), many of which are known to make direct contacts with BC-L5PNs (Agmon and Connors, 1992;Constantinople and Bruno, 2013;El-Boustani et al, 2020;Rodriguez-Moreno et al, 2020). The presence or absence of a Ca 2+ spike in evoked action potentials allowed us to classify BC-L5PNs as either A-type or B-type.…”

“…Sensory information is received in the barrel cortex from different nuclei of the thalamus. Among these nuclei, ventral posterior medial nucleus, ventrobasal nucleus, and posterior medial nucleus are known to directly innervate layer 5 pyramidal neurons (BC-L5PNs) (Agmon and Connors, 1992;Constantinople and Bruno, 2013;El-Boustani et al, 2020;Rodriguez-Moreno et al, 2020). In basal dendrites of BC-L5PN, coactivation of neighboring dendritic inputs can initiate NMDAR-mediated dendritically-restricted spikes characterized by large Ca 2+ transients and long-lasting depolarizations (Nevian et al, 2007;Polsky et al, 2009;Schiller et al, 2000), providing the appropriate environment for BK activation.…”

Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response

“…Interestingly, in a related whisker detection task without a delay period, enhanced reciprocal signaling between wS1 and wS2 has already been proposed to play an important role (Kwon et al, 2016;Yamashita and Petersen, 2016). It is also important to note that a large number of subcortical structures are also likely to be involved in task performance including thalamus (El-Boustani et al, 2020;Guo et al, 2017), basal ganglia (Sippy et al, 2015) and cerebellum (Chabrol et al, 2019;Gao et al, 2018).…”