Tactile directional sensibility: peripheral neural mechanisms in man

doi:10.1016/S0006-8993(00)02278-2

Brain Research

Volume 866, Issues 1–2, 2 June 2000, Pages 178-187

https://doi.org/10.1016/S0006-8993(00)02278-2 Get rights and content

Abstract

Tactile directional sensibility, i.e. the ability to tell the direction of an object’s motion across the skin, is an easily observed sensory function that is highly sensitive to disturbances of the somatosensory system. Based on previous psychophysical experiments on healthy subjects it was concluded that directional sensibility depends on two kinds of information from cutaneous mechanoreceptors; spatio-temporal information and information about friction-induced changes in skin stretch. In the present study responses to similar probe movements as in the psychophysical experiments were recorded from human single mechanoreceptors in the forearm skin. All slowly adapting type 2 (SA2) units were spontaneously active, and with increasing force of friction their discharge rates were modified by probe movements at increasing distances from the Ruffini end-organ, reflecting the high stretch-sensitivity of these units. Slowly adapting type 1 (SA1) and field units responded to the moving probe within well-defined skin areas directly overlying the individual receptor terminals, and compared to the SA2 units their response properties were less dependent on the force of friction. The results suggest that SA1 and field units have the capacity to signal spatio-temporal information, whereas a population of SA2 units have the capacity to signal direction-specific information about changes in lateral skin stretch.

Introduction

The ability to tell the direction of an object’s motion across the skin is an easily observed sensory function that appears to be fairly selectively vulnerable to damages of the somatosensory pathway, all the way from the peripheral receptors to the cerebral cortex [2], [7], [14], [18], [24], [27]. Consequently, assessment of tactile directional sensibility has been recommended as a standard method for evaluation of patients with somatosensory disturbances [2], [14]. A detailed knowledge of the underlying neural mechanisms is a prerequisite for correct interpretation of the results, as well as for providing guidelines for the optimal testing procedure.

In theoretical studies, considerable interest has been focused on the brain’s capacity to infer the direction of motion on the basis of spatio-temporal information; i.e. information about the temporal order of activation of adjacent cutaneous mechanoreceptors [4], [6], [8], [9], [10]. However, besides spatio-temporal information the brain may also utilize another type of sensory data for directional sensibility. Gould et al. [11] reported that directional sensibility was better for a stimulus that caused friction between the moving object and the skin compared to an air-stream stimulus. In our laboratory we confirmed the findings of Gould et al. and showed that for the stimulus that caused friction, but not for the air-stream stimulus, the accuracy of directional sensibility was positively correlated to the indentation force [19], [22]. Based on this and other evidence it was concluded that directional sensibility might depend on the parallel processing of two different types of sensory information. One consists of spatial data that vary with time and the other consists of direction-specific responses, induced by friction, from afferents sensitive to changes in skin stretch [22].

Many of the above psychophysical experiments were made in the forearm skin of humans. Five types of mechanoreceptors with myelinated afferents, i.e. SA1 (slowly adapting type 1, Merkel), SA2 (slowly adapting type 2, Ruffini), hair units, field units, and PC (Pacini) units have been identified in that skin region, and their receptive field structures have been described in detail [26].

The aim of the present investigation was to study how the different types of myelinated mechanoreceptors in the forearm skin may contribute to directional sensibility. The skin was stimulated by the same probe movements as in one of the psychophysical experiments [22], and recordings were simultaneously made from single units. It will be shown that SA1 and field units have the capacity to signal spatio-temporal information, whereas a population of SA2 units may provide direction-specific information about changes in lateral skin stretch.

A preliminary report of part of this work has previously been published in abstract form [21].

Section snippets

Material and methods

Mechanoreceptive units with rapidly conducting afferents and receptive fields in the forearm skin were studied in 18 experiments on healthy volunteers; seven females and ten males, 22–31 years old. Informed consent was obtained, the study was performed according to the Declaration of Helsinki, and the Ethical Committee of the Medical Faculty, Göteborg University, approved the procedure.

Results

Thirty-one fast-conducting afferents with mechanoreceptors located in the forearm skin were studied. The receptive fields were evenly distributed between the wrist and cubital fold on the radial and posterior surfaces of the forearm. The units were separated into four types on the basis of the criteria described in Methods, i.e. (i) slowly adapting type 1 (SA1, Merkel, n=8), (ii) slowly adapting type 2 (SA2, Ruffini, n=12), (iii) hair units, rapidly adapting (n=7), and (iv) field units, rapidly

Discussion

Previous psychophysical experiments have shown that tactile directional sensibility is dependent on the parallel processing of spatial information expressed as a function of time and information about friction-induced changes in skin stretch [11], [19], [22]. We have now found that SA1 and field units may signal spatio-temporal information, whereas a population of SA2 units may signal friction-induced changes in skin stretch.

Acknowledgements

This study was supported by the Swedish Medical Research Council (Grant 14X-3548), the Swedish Society of Medicine, and the Magn Bergvall foundation. Drs. Åke Vallbo and Ulf Norrsell kindly read and advised on a previous version of the text. We would like to thank Sven-Öjvind Swahn for valuable technical support.

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Research reportTactile directional sensibility: peripheral neural mechanisms in man

Abstract

Introduction

Section snippets

Material and methods

Results

Discussion

Acknowledgements

J. Neurol. Sci.

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Brain Res. Rev.

Prog. Biophys. Mol. Biol.

Random Data

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J. Neurosci.

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Research report
Tactile directional sensibility: peripheral neural mechanisms in man