Identification of a Developmental Switch in Information Transfer between Whisker S1 and S2 Cortex in Mice

Abstract

The whiskers of rodents are a key sensory organ that provides critical tactile information for animal navigation and object exploration throughout life. Previous work has explored the developmental sensory-driven activation of the primary sensory cortex processing whisker information (wS1), also called barrel cortex. This body of work has shown that the barrel cortex is already activated by sensory stimuli during the first postnatal week. However, it is currently unknown when over the course of development these stimuli begin being processed by higher-order cortical areas, such as secondary whisker somatosensory area (wS2). Here we investigate the developmental engagement of wS2 by whisker stimuli and the emergence of corticocortical communication from wS1 to wS2. Using in vivo wide-field imaging and multielectrode recordings in control and conditional KO mice of either sex with thalamocortical innervation defects, we find that wS1 and wS2 are able to process bottom-up information coming from the thalamus from birth. We also identify that it is only at the end of the first postnatal week that wS1 begins to provide functional excitation into wS2, switching to more inhibitory actions after the second postnatal week. Therefore, we have uncovered a developmental window when information transfer between wS1 and wS2 reaches mature function. SIGNIFICANCE STATEMENT At the end of the first postnatal week, the primary whisker somatosensory area starts providing excitatory input to the secondary whisker somatosensory area 2. This excitatory drive weakens during the second postnatal week and switches to inhibition in the adult.

Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse

“…In contrast, between S1Bf and S2 only a very weak temporal correlation between the bursts and no significant directionality of burst onsets were observed. This finding suggests that only a weak synaptic connection exists between S1 and S2 in the early postnatal brain, which is in line with a recent in vivo study demonstrating that whisker-related activity in the S2 regions is smaller and that a consistent activity representing a solid interaction between both areas establishes only around P6 ( Cai et al, 2022 ). Importantly, the significant information transfer from S1Bf to M1 occurred both between L5/6 and between the SP, while the connection from S1Bf SP to M1 L5/6 is less prominent ( Figure 7 and Table 4 ).…”

“…In contrast to this connection between S1Bf and M1, our experimental results indicate that the functional connectivity between S1 and S2 is less developed at P0, although we observed in the SP anatomical projections between S2 and S1Bf. Correlated neuronal activity occurs in this region at P6-8 ( Cai et al, 2022 ), suggesting that the connectivity toward secondary sensory areas develops delayed, as has been also shown for associative cortical areas ( Sydnor et al, 2021 ).…”

“…The establishment of the functional connectivity between S1 and M1 was previously demonstrated, showing that M1 is involved in somatosensory information processing during early development [between postnatal day 3 and 12 (P3-12)] in the rat ( An et al, 2014 ; Dooley and Blumberg, 2018 ; Gomez et al, 2021 ). Functional connections between S1 and S2 appear around the end of the first postnatal week ( Cai et al, 2022 ). No information is currently available on anatomical and functional connectivity between S1, S2, and M1 in mouse at the earliest postnatal stages.…”

Cortical networks show characteristic recruitment patterns after somatosensory stimulation by pneumatically evoked repetitive hand movements in newborn infants

“…The exact mechanistic underpinnings of the development of CKC responses and their cortico-cortical spread are as yet poorly understood at the cellular level. However, related studies on animal models have shown that higher-order somatosensory cortical areas become responses to thalamic sensory input at the end of the first postnatal week ( Cai et al. 2022 ).…”

A nasal chemosensation–dependent critical window for somatosensory development

“…Together with nasal chemosensation, somatosensation is also functional at birth (15)(16)(17), and it is only at around postnatal day (P) 11 and P14 that mice begin processing external auditory and visual information, respectively (18)(19)(20)(21)(22). Therefore, nasal chemosensation and somatosensation work in tandem to allow neonates to perceive the world (7,16,23) and also cross-modally regulate other senses to affect adult behavior (23)(24)(25).…”