Elsevier

Brain Research

Volume 815, Issue 2, 9 January 1999, Pages 326-336
Brain Research

Research report
EEG evidence of stimulus-directed response dynamics in human somatosensory cortex

https://doi.org/10.1016/S0006-8993(98)01087-7Get rights and content

Abstract

Dense multichannel recordings of scalp electroencephalogram (EEG) were obtained in the vicinity of primary somatosensory cortex, time-locked to repetitive vibrotactile stimulation of sites on the right index finger of a single human subject. Frequency-domain analysis of cross-trial averages revealed prominent `driving' responses in the EEG at the frequency of stimulation, which under specific stimulus conditions displayed pronounced changes in amplitude and topographic organization over brief (4 s) durations of stimulus exposure. The changes were systematic and physiologically coherent, evolving toward driving-response topographies observed in the same subject in conjunction with periodic microstimulation of single mechanoreceptive afferents whose receptive fields occupied corresponding positions on the digit. This dynamic process was orderly and reproducible, and could be controlled by manipulating factors such as the amplitude, frequency, and temporal spacing of the stimuli. The results are tentatively interpreted in light of a previously proposed neurophysiological model of stimulus-driven response plasticity in mammalian somatosensory cortex.

Introduction

Vibrotaction, the sensory response to vibrotactile stimuli, provides a rich arena for experimental investigations of sensory neurophysiology. A great deal is already known about the responses of single units at levels ranging from mechanoreceptive afferents to the cortical entry stage, and there is a large psychophysical literature related to judgments by humans and other primates of the presence, magnitude, and frequency of vibrotactile stimuli (e.g., Refs. 6, 18, 21, 24, 25, 30, 34, 39, 48, 53).

Traditional neurophysiological accounts have generally emphasized the fidelity of the neural response to vibrotactile stimuli, expressed in the form of driving or frequency-following responses (FFRs)—i.e., entrainment of the spike discharge activity of the responding neural population at the driving frequency (and sometimes its low harmonics). However, attention has recently turned toward plasticity of the response at the cortical level, and to the possibility that the well-documented improvements in amplitude and frequency discrimination which accompany prolonged vibrotactile stimulation 16, 17, 22may be mediated in substantial part by dramatic, reversible, and reproducible changes that such stimulation has been shown to produce in large-scale patterns of neuronal response in primary somatosensory cortex 51, 55, 56.

A detailed review of existing studies of the effects of repeated or prolonged stimulation on properties of the somatosensory evoked potential (SEP) strongly suggested that these large-scale cortical dynamic processes should be accessible to non-invasive study in humans using high-resolution electroencephalogram (EEG) techniques 33, 57. In pursuit of this goal, our laboratory is carrying out intensive within-subject studies which combine vibrotactile stimulation of the digits with extraction of FFRs from dense multichannel recordings of EEG obtained from a scalp region overlying and surrounding the SI representational field of the hand. These FFRs are small compared with the overall amplitude of background EEG, but they are much larger relative to background amplitudes at the driving frequencies, and thus lend themselves to measurement using frequency-domain methods [42].

In a previous paper we used these techniques to demonstrate that periodic microstimulation of single mechanoreceptive afferents in the median nerve of a human subject produced driving responses of physiological origin in the associated EEG [29]. Furthermore, the scalp topography of these responses varied systematically and dramatically as a function of the location on the hand of the receptive field of the stimulated unit. In the present paper we show how these microstimulation results have illuminated the physiological coherence of rapid changes in response topography that accompany vibrotactile stimulation of the hand in the same subject.

Section snippets

Materials and methods

The main findings to be presented were developed in the course of a series of more than 30 experiments carried out during a seven-month period, all with a single volunteer subject, one of the authors (EFK). All experiments used the general methods described in this section, with specific session-by-session adjustments identified in the narrative that accompanies the presentation of results.

Results

The first three studies were intended to provide information about basic properties of the driving response under ostensibly non-adapting conditions. All three used the volar tip of right digit two as the site of stimulation, with a contactor diameter of 8 mm, stimulus frequency of 27 Hz, and peak stimulus amplitudes of 50, 100, 200, and 400 μm. Each experiment consisted of thirty-five or forty 4-s exposures to each of the four amplitudes, in random order and with a base interstimulus interval

Discussion

Two main findings are firmly established for our principal subject by the results presented here: First, the topography of the scalp-recorded driving response induced by a moderate to strong vibrotactile stimulus applied to the hand is not constant, but changes with time and in a manner dependent on the recent history of stimulation. The aggregate first-order driving response measured at the level of the wrist, however, shows no consistent change in amplitude across time, and no sign of

Acknowledgements

We thank our colleagues W. Maixner, D. McLaughlin, and B. Whitsel for reviewing earlier versions of this paper. The research was supported by the National Institute of Dental Research, Grant DE-07509 to E. Kelly.

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