Synchrony within Aβ mechanoreceptor subtypes governs signal propagation to primary somatosensory cortex
Abstract
Fast-conducting A{beta} slowly adapting type I low threshold mechanoreceptors (SAI-LTMRs) and A{beta} 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 A{beta} 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 patterns in individual A{beta} LTMR subtypes. Here, we took advantage of a fast variant of channelrhodopsin, CatCh, which enabled us to generate physiological spiking rates and patterns 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 A{beta} SAI-LTMRs to neural activity (spiking and local field potential) in S1 is dependent on synchronous activation of multiple A{beta} SAI-LTMRs. Asynchronous activation of the same A{beta} 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 A{beta} SAI-LTMRs during static indentations contribute to the preponderance of transient cortical responses. By contrast, both synchronous and asynchronous activation of multiple A{beta} RAI-LTMRs resulted in robust S1 responses. Overall, the temporal patterning and synchrony of activity within A{beta} LTMR subtypes govern how well their signals propagate through the ascending somatosensory system. Key PointsO_LICatCh, a sensitive and fast channelrhodopsin variant, enables pulsed-light generation of physiological spiking patterns in A{beta} low threshold mechanoreceptor (LTMR) subtypes. C_LIO_LIThe synchrony of multiple mechanoreceptors within a subtype controls the extent to which their signals influence activity in primary somatosensory cortex. C_LIO_LIA{beta} rapidly adapting type I (RAI-) LTMRs drive stronger cortical responses than A{beta} slowly adapting type I (SAI-) LTMRs, especially when considering asynchronous activation of A{beta} LTMRs within each subtype. C_LI
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