Layer 4 barrel cortex neurons retain their response properties during whisker replacement.

Abstract

Bodies change continuously, but we do not know if and how these changes affect somatosensory cortex. We address this issue in the whisker-barrel-cortex-pathway. We ask how outgrowing whiskers are mapped onto layer 4 barrel neuron responses. Half of whisker follicles contained dual whiskers, a shorter presumably outgrowing whisker (referred to as young whisker) and a longer one (referred to as old whisker). Young whiskers were much thinner than old ones but were inserted more deeply into the whisker follicle. Both whiskers were embedded in one outer root sheath surrounded by a common set of afferent nerve fibers. We juxtacellularly identified layer 4 barrel neurons representing dual whiskers with variable whisker length differences in anesthetized rats. Strength and latency of neuronal responses were strongly correlated for deflections of young and old whiskers but were not correlated with whisker length. The direction preferences of young and old whiskers were more similar than expected by chance. Old whiskers evoked marginally stronger and slightly shorter latency spike and local field potential responses than young whiskers. Our data suggest a conservative rewiring mechanism, which connects young whiskers to existing peripheral sensors. The fact that layer 4 barrel neurons retain their response properties is remarkable given the different length, thickness, and insertion depth of young and old whiskers. Retention of cortical response properties might be related to the placement of young and old whisker in one common outer root sheath and may contribute to perceptual stability across whisker replacement. NEW & NOTEWORTHY A particularly dramatic bodily change is whisker regrowth, which involves the formation of dual whisker follicles. Our results suggest that both whiskers are part of the same mechanoreceptive unit. Despite their distinct whisker length and thickness, responses of single cortical neurons to young and old whisker deflection were similar in strength, latency, and directional tuning. We suggest the congruence of young and old whisker cortical responses contributes to perceptual stability over whisker regrowth.