Elsevier

Brain Research

Volume 1102, Issue 1, 2 August 2006, Pages 109-116
Brain Research

Research Report
Vibrotactile adaptation enhances spatial localization

https://doi.org/10.1016/j.brainres.2006.05.037Get rights and content

Abstract

A two-interval forced choice tracking procedure was used to evaluate the effects of a pre-exposure to vibrotactile stimulation (“adaptation”) on the capacity of human subjects to spatially localize a subsequent tactile stimulus. A 25 Hz flutter adapting stimulus was presented at a randomly selected position within a 20 mm linear array oriented transversely on the hand dorsum. Two flutter stimuli delivered subsequently were applied to different sites along the linear array; one to the same locus that received the adapting stimulation (the “standard” stimulus), the other to a distant site (the “test” stimulus). Following each trial, subjects were queried as to which of the two stimuli was delivered to the same skin site that received adapting stimulation. A correct response resulted in a reduced distance between the sites contacted by the standard and test stimuli in the following trial. Four subjects participated in 10 sessions each. A session consisted of two sets of 20 trials (one set at 0.5 s and another at 5 s adapting stimulus duration). For every subject, 5 s adaptation resulted in an approximately 2-fold improvement in spatial discrimination performance over that achieved following 0.5 s adaptation. It is proposed that the improved human vibrotactile spatial localization performance following 5 s of 25 Hz stimulation is due to enhanced spatial funneling of the global neuronal population response of primary somatosensory cortex (SI) that has been demonstrated to accompany increases in duration of 25 Hz flutter stimuli delivered to the skin.

Introduction

Extended exposure to continuous vibrotactile stimulation (“vibrotactile adaptation”) at a discrete skin site not only elevates vibrotactile detection threshold, but decreases the subjective magnitude of suprathreshold stimuli whose physical attributes are similar to those of the adapting stimulus (Bensmaia and Hollins, 2000, Burton et al., 1998, Delemos and Hollins, 1996, Gescheider et al., 2004). Although the neural mechanisms that underlie these perceptual effects of a pre-exposure to vibrotactile stimulation remain to be established with absolute certainty, animal studies have demonstrated that such a pre-exposure is reliably accompanied by reductions in neuronal responsivity at both peripheral and central levels of the somatosensory nervous system. For example, multi-second vibrotactile stimulation is accompanied by a sustained decrease of the responsivity of skin mechanoreceptors located in the vicinity of the stimulated skin region (Leung, 1995), a long-lasting depression of the responsivity of neurons in the cuneate nucleus of the brainstem ipsilateral to the stimulus site (O'Mara et al., 1988), and a decrease of the spatial extent of the SI region activated by mechanical stimulation of a discrete skin site (Juliano et al., 1981, Juliano et al., 1983). Other studies have shown that, despite the above-described decreases in the responsivity of somatosensory afferents and CNS neurons, vibrotactile adaptation is followed by significant improvement of the capacity of subjects to discriminate the amplitude and frequency of vibrotactile stimuli when the frequencies of the adapting and standard stimuli are similar (Delemos and Hollins, 1996, Goble and Hollins, 1993, Goble and Hollins, 1994, Tommerdahl et al., 2005). When the frequencies of the adapting and standard stimuli are substantially different (e.g., 25 Hz adaptation followed by test frequencies in the vicinity of 200 Hz), however, human vibrotactile frequency discriminative capacity is significantly degraded following adaptation (Tommerdahl et al., 2005).

Observations obtained in recent optical intrinsic signal (OIS) imaging studies which used different durations of vibrotactile stimulation have raised the intriguing possibility that the very different SI cortical activity patterns evoked by long- vs. short-duration contralateral skin flutter stimulation might support very different vibrotactile spatial localization capacities. More specifically, Simons et al. (2005) reported that the response of SI (squirrel monkey) recorded after 5 s of 25 Hz skin flutter stimulation is characterized not only by an increase in activity in the region that receives short-latency input from the stimulated skin region, but also by a prominent decrease in activity in the surrounding region which is not observed when stimulus duration is 0.5 s or shorter. This discrepancy between the responses evoked in contralateral SI cortex by long- vs. short-duration skin flutter stimulation, together with the prominent poststimulus persistence of the decrease in activity a flutter stimulus evokes in the territory that surrounds the stimulus-activated region in SI (Simons et al., 2005) strongly suggested that the SI response (and presumably, therefore, the perceptual experience) evoked by a skin flutter stimulus applied to the same or a neighboring skin site would be significantly altered if the stimulus was applied within a few seconds after a preceding exposure (at least 5 sec in duration) to 25 Hz stimulation. Furthermore, if as is widely believed, the ability to spatially localize a tactile stimulus is determined by the locus of stimulus-evoked activation within SI, it seemed likely that pre-exposure to a 5 s flutter stimulus would alter both the SI response to a flutter stimulus applied subsequently to a nearby skin site as well as the perceived location of that stimulus. This study evaluated the latter expectation using a two-interval forced-choice (2IFC) tracking paradigm to characterize the ability of human subjects to localize the site of skin flutter stimulation subsequent to 5 s vs. 0.5 s vibrotactile adaptation.

Section snippets

Results

A two-interval forced-choice (2IFC) tracking protocol was used to determine spatial localization threshold under two different durations of adapting stimulation (5 s vs. 0.5 s). Exemplary results for one session (two runs) for each of the four subjects are shown in Fig. 1. Note that under the condition with a 0.5 s adapting stimulus, the subjects were able to correctly localize the points at a distance of approximately 8–9 mm as indicated by the tracking plots. When the adapting stimulus

Discussion

In the present study, we observed the effects of adaptation on spatial localization of a 25 Hz flutter stimulus on the dorsal surface of the attended hand. The localization tracking distance was greatly reduced (i.e., spatial acuity was improved) with a 5 s adapting stimulus compared to that with a 0.5 s adapting stimulus. Specifically, it was found that long-duration adaptation resulted in improved spatial acuity by nearly 2-fold relative to the short-duration adaptation condition. To our

Experimental procedures

Four subjects (20–29 years in age) were studied who were naive both to the study design and issue under investigation. All procedures were reviewed and approved in advance by an institutional review board.

Sinusoidal vertical skin displacement stimuli were delivered to the dorsum of the hand using a vertical displacement stimulator (Cantek Metatron Corp., Canonsburg, PA) fitted with a Two-Point Stimulator (TPS). The TPS and its use are described in detail in two separate reports (Tannan et al.,

Acknowledgments

This work was supported, in part by NIH R01 grant NS043375 (M. Tommerdahl, P.I.). VT received salary support from NIH grant NS045685.

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