Synchrony within Aβ mechanoreceptor subtypes governs signal propagation to primary somatosensory cortex

Abstract

Fast-conducting Aβ slowly adapting type I low threshold mechanoreceptors (SAI-LTMRs) and Aβ rapidly adapting type I (RAI-) LTMRs are critical for discriminative touch from glabrous skin. Recent studies used mouse genetic loss-of-function and optogenetic gain-of-function manipulations to determine that signals from these Aβ LTMRs are integrated subcortically to build the cortical representation of touch. However, the precise influence of each subtype on downstream responses is unclear, in part because previous manipulations lacked the capacity to reproduce physiological firing rates and patterns in individual Aβ LTMR subtypes. Here, we took advantage of a fast variant of channelrhodopsin, CatCh, which enabled us to generate irregular spike trains with mean rates of 20 Hz in either subtype while monitoring responses in mouse primary somatosensory cortex (S1). Doing so revealed that propagation of steady-state signals from sustained responses of Aβ SAI-LTMRs to neural activity (spiking and local field potential) in S1 is dependent on synchronous activation of multiple Aβ SAI-LTMRs. Asynchronous activation of the same Aβ SAI-LTMRs rarely produced sustained responses in S1 measured at the level of single unit spiking as well as local field potentials. This suggests that the irregular firing patterns of Aβ SAI-LTMRs during static indentations contribute to the preponderance of transient cortical responses. By contrast, both synchronous and asynchronous activation of multiple Aβ RAI-LTMRs resulted in robust S1 responses. Overall, the temporal patterning and synchrony of activity within Aβ LTMR subtypes govern how well their signals propagate through the ascending somatosensory system. Abstract Figure Legend We used an optogenetic gain-of-function manipulation to investigate how sensory signals from two subtypes of Aβ LTMRs contribute to the cortical representation of touch. CatCh, a sensitive and fast channelrhodopsin variant, enables pulsed-light generation of high-frequency action potential trains in Aβ LTMR subtypes. Synchronous activation of Aβ LTMRs generated larger responses, especially when considering sustained activity, than asynchronous activation. This suggests that the temporal patterning and synchrony of activity within Aβ LTMR subtypes govern how well their signals propagate through the ascending somatosensory system.