ASICs mediate fast excitatory synaptic transmission for tactile discrimination

Tactile discrimination, the ability to differentiate objects’ physical properties such as texture, shape, and edges, is essential for environmental exploration, social interaction, and early childhood development. This ability heavily relies on Merkel cell-neurite complexes (MNCs), the tactile end-organs enriched in the fingertips of humans and the whisker hair follicles of non-primate mammals. Although recent studies have advanced our knowledge on mechanical transduction in MNCs, it remains unknown how tactile signals are encoded at MNCs. Here, using rodent whisker hair follicles, we show that tactile signals are encoded at MNCs as fast excitatory synaptic transmission. This synaptic transmission is mediated by acid-sensing ion channels (ASICs) located on the neurites of MNCs, with protons as the principal transmitters. Pharmacological inhibition or genetic deletion of ASICs diminishes the tactile encoding at MNCs and impairs tactile discrimination in animals. Together, ASICs are required for tactile encoding at MNCs to enable tactile discrimination in mammals. [Display omitted] •Merkel cell-neurite complexes (MNCs) encode tactile signals using synaptic transmission•This synaptic transmission is mediated by acid-sensing ion channels (ASICs) on MNCs•Protons serve as the principal transmitters for synaptic transmission at MNCs•ASICs play a role in the sense of touch and tactile discrimination in mammals Yamada et al. show that acid-sensing ion channels (ASICs) mediate fast excitatory synaptic transmission at the tactile end organs, Merkel cell-neurite complexes (MNCs), with protons serving as the principal transmitters. This suggests the unique role of ASICs in the sense of touch and tactile discrimination in mammals.