Research Article

Meissner corpuscles and their spatially intermingled afferents underlie gentle touch perception

See allHide authors and affiliations

Science  19 Jun 2020:
Vol. 368, Issue 6497, eabb2751
DOI: 10.1126/science.abb2751

You are currently viewing the abstract.

View Full Text

Log in to view the full text

Log in through your institution

Log in through your institution

Secrets of Meissner corpuscles

The Meissner corpuscle, a mechanosensory end organ, was discovered more than 165 years ago and has since been found in the glabrous skin of all mammals, including that on human fingertips. Although prominently featured in textbooks, the function of the Meissner corpuscle is unknown. Neubarth et al. generated adult mice without Meissner corpuscles and used them to show that these corpuscles alone mediate behavioral responses to, and perception of, gentle forces (see the Perspective by Marshall and Patapoutian). Each Meissner corpuscle is innervated by two molecularly distinct, yet physiologically similar, mechanosensory neurons. These two neuronal subtypes are developmentally interdependent and their endings are intertwined within the corpuscle. Both Meissner mechanosensory neuron subtypes are homotypically tiled, ensuring uniform and complete coverage of the skin, yet their receptive fields are overlapping and offset with respect to each other.

Science, this issue p. eabb2751; see also p. 1311

Structured Abstract

INTRODUCTION

Meissner corpuscles are mechanosensory end organs that densely occupy mammalian glabrous skin. The basic anatomy of the Meissner corpuscle and the Aβ (large soma diameter and fast action potential conducting) mechanosensory neurons that innervate it have been widely described. However, little is known about the requirement for the Meissner corpuscle and its innervating Aβ mechanosensory neurons for touch-related behaviors, sensorimotor capabilities, and tactile perception.

RATIONALE

Mice lacking either brain-derived neurotrophic factor (BDNF) or its receptor TrkB have a range of developmental deficits, including an absence of Meissner corpuscles. We reasoned that confining TrkB manipulations to sensory neurons in conjunction with selective genetic labeling approaches would allow us to investigate the developmental assembly of Meissner corpuscles and their functions in somatosensation. While examining Meissner corpuscle development, we found that two Aβ mechanosensory neuron types innervate the corpuscle. Here, we assessed the requirement of Meissner corpuscles for touch sensitivity and fine sensorimotor control and the anatomical, physiological, and ultrastructural properties of the two Aβ sensory neurons that innervate this mechanosensory end organ.

RESULTS

Sensory neuron–specific knockout of TrkB resulted in complete loss of Meissner corpuscles without affecting other mechanosensory end organs in mouse glabrous (nonhairy) skin, including Aβ mechanosensory neuron–Merkel cell complexes and Pacinian corpuscles. Behavioral measurements showed that mice lacking Meissner corpuscles were deficient in perceiving and reacting to the gentlest detectable forces acting on glabrous skin and in fine sensorimotor control.

Genetic labeling experiments revealed that Meissner corpuscles are innervated by two molecularly distinct Aβ sensory neuron types, one that expresses TrkB and the other that expresses the tyrosine kinase Ret. Despite innervating the same end organ, the responses of these two Aβ neuron types to tactile stimuli differed: The TrkB-positive (TrkB+) Meissner afferent was more sensitive and responded at both the onset and the offset of step indentations of glabrous skin, whereas the Ret+ Meissner afferent was less sensitive and rarely responded at step offset. Some Ret+ neurons even had sustained responses during a static indentation stimulus. In addition, the axonal endings of these two Aβ mechanosensory neuron types were found to be homotypically tiled but heterotypically offset. Computational modeling suggested that this anatomical arrangement maximizes information available for encoding acuity while ensuring complete coverage of the skin using a limited number of neurons. Finally, ultrastructural analysis using electron microscopy revealed that the axon terminals of the more sensitive TrkB+ Meissner afferents had greater numbers of lamellar cell wrappings than the terminals of the less sensitive Ret+ Meissner afferents.

CONCLUSION

We conclude that two homotypically tiled but heterotypically offset Aβ mechanosensory neurons with distinct molecular, physiological, and ultrastructural properties innervate Meissner corpuscles, which underlie the perception of, and behavioral responses to, the gentlest detectable forces acting on glabrous skin.

Anatomy and physiology of Meissner corpuscles required for tactile behavior.

(A to C) Meissner corpuscles and their Aβ afferents (A) were required for normal tactile sensitivity (B) and fine sensorimotor control (C). (D) TrkB+ and Ret+ Aβ neurons both innervated Meissner corpuscles. (E and F) TrkB+ Meissner afferents were more sensitive (E) and had more lamellar cell wrappings [(F), arrows indicate axons wrapped with lamellar processes] compared with Ret+ Meissner afferents. In (A), S100 and NFH are antibodies used to visualize Meissner corpuscles and their afferents, respectively. In (B) and (C), error bars represent SEM, and *p < 0.05, **p < 0.01, and ***p < 0.001.

Abstract

Meissner corpuscles are mechanosensory end organs that densely occupy mammalian glabrous skin. We generated mice that selectively lacked Meissner corpuscles and found them to be deficient in both perceiving the gentlest detectable forces acting on glabrous skin and fine sensorimotor control. We found that Meissner corpuscles are innervated by two mechanoreceptor subtypes that exhibit distinct responses to tactile stimuli. The anatomical receptive fields of these two mechanoreceptor subtypes homotypically tile glabrous skin in a manner that is offset with respect to one another. Electron microscopic analysis of the two Meissner afferents within the corpuscle supports a model in which the extent of lamellar cell wrappings of mechanoreceptor endings determines their force sensitivity thresholds and kinetic properties.

View Full Text

Stay Connected to Science