Abstract

SummaryThe deep dorsal horn is a poorly characterized spinal cord region implicated in processing low-threshold mechanoreceptor (LTMR) information. We report an array of mouse genetic tools for defining neuronal components and functions of the dorsal horn LTMR-recipient zone (LTMR-RZ), a role for LTMR-RZ processing in tactile perception, and the basic logic of LTMR-RZ organization. We found an unexpectedly high degree of neuronal diversity in the LTMR-RZ: seven excitatory and four inhibitory subtypes of interneurons exhibiting unique morphological, physiological, and synaptic properties. Remarkably, LTMRs form synapses on between four and 11 LTMR-RZ interneuron subtypes, while each LTMR-RZ interneuron subtype samples inputs from at least one to three LTMR classes, as well as spinal cord interneurons and corticospinal neurons. Thus, the LTMR-RZ is a somatosensory processing region endowed with a neuronal complexity that rivals the retina and functions to pattern the activity of ascending touch pathways that underlie tactile perception.

Highlights

  • The somatosensory system decodes a wide range of tactile stimuli, thereby endowing us with an extraordinary capacity for object recognition, texture discrimination, and fine motor control

  • Guard hair follicles are associated with Ab RA-low-threshold mechanoreceptor (LTMR), Ab SAI-LTMRs, and Ab Field-LTMRs, which are differentially sensitive to hair deflection, skin indentation, and stroke and exhibit different rates of adaptation (Abraira and Ginty, 2013; Burgess et al, 1968)

  • Through an openended screen to identify genes that are uniquely expressed in select LTMR-recipient zone (LTMR-RZ) neuronal subtypes, and exploitation of these genes for the generation of an array of mouse molecular-genetic tools, we found within the LTMR-RZ seven excitatory and four inhibitory interneuron subtypes, each displaying a unique combination of morphological and physiological properties

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Summary

Introduction

The somatosensory system decodes a wide range of tactile stimuli, thereby endowing us with an extraordinary capacity for object recognition, texture discrimination, and fine motor control. The unique morphological and anatomical arrangement of LTMR subtype endings in the skin, our largest sensory organ, underlies distinct LTMR subtype response properties for the perception of object size, shape, texture, vibration, and direction of stimulus movement (Owens and Lumpkin, 2014; Zimmerman et al, 2014). LTMRs are further distinguished by their preferred stimuli, the cutaneous end organs with which they associate, and by their rates of adaptation to constant indentation of the skin. The perception of diverse tactile stimuli requires robust and precise mechanical stimulus detection by LTMR peripheral endings in the skin and intricate processing capabilities of LTMR activity ensembles by interneurons in the CNS. Defining the cellular and synaptic substrates of touch information processing in the CNS will reveal how LTMR activity ensembles, internal state, and experience are integrated to generate percepts of the physical world

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