Research ReportVibrotactile adaptation enhances spatial localization
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.
References (30)
- et al.
Some characteristics of tactile channels
Behav. Brain Res.
(2004) - et al.
Functional imaging of perceptual learning in human primary and secondary somatosensory cortex
Neuron
(2003) - et al.
Spatial discrimination thresholds for pain and touch in human hairy skin
Pain
(2001) - et al.
A novel device for delivering two-site vibrotactile stimuli to the skin
J. Neurosci. Methods
(2005) - et al.
Human vibrotactile frequency discriminative capacity after adaptation to 25 Hz to 200 Hz stimulation
Brain Res.
(2005) - et al.
Complex tactile waveform discrimination
J. Acoust. Soc. Am.
(2000) - et al.
Vibrotactile stimulus order effects in somatosensory cortical areas of rhesus monkeys
Somatosens. Motor Res.
(1998) - et al.
Stimulus-dependent spatial patterns of response in SI cortex
BMC Neurosci.
(2005) - et al.
Adaptation-induced enhancement of vibrotactile amplitude discrimination: the role of adapting frequency
J. Acoust. Soc. Am.
(1996) - et al.
Vibrotactile adaptation enhances amplitude discrimination
J. Acoust. Soc. Am.
(1993)
Vibrotactile adaptation enhances frequency discrimination
J. Acoust. Soc. Am.
Patterns of increased metabolic activity in the somatosensory cortex of monkeys subjected to controlled cutaneous stimulation: a 2-deoxyglucose study
J. Neurophysiol.
Patterns of metabolic activity in cytoarchitectural area SII and surrounding cortical fields of the monkey
J. Neurophysiol.
Capacities of humans and monkeys to discriminate between vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychophysical measurements
J. Neurophysiol.
Disorders in somesthesis following lesions of parietal lobe
J. Neurophysiol.
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2016, NeuronCitation Excerpt :More than half a century ago, von Békésy noted that the perceived size of a tactile stimulus decreased with increasing frequency of a repetitive sensory stimulus (von Békésy, 1957). Perceptual studies in human tactile sensing further suggested that somatosensory adaptation enhanced spatial discrimination between stimuli through vibrotactile input to the fingertip (Goble and Hollins, 1993, 1994; Tannan et al., 2006; Vierck and Jones, 1970), and subsequent studies have investigated the spatial sharpening of representations in somatosensory cortex in response to repetitive, ongoing sensory inputs (Lee and Whitsel, 1992; Moore et al., 1999; Sheth et al., 1998; Simons et al., 2005; Tommerdahl et al., 2002), posited as a potential explanation for enhanced spatial acuity (Lee and Whitsel, 1992; Moore et al., 1999; Vierck and Jones, 1970). These results have been expanded to investigate the underlying neural correlates of spatial discrimination in multiple animals models of somatosensation, including the monkey fingertip (Simons et al., 2005) and the rodent vibrissa pathway (Ollerenshaw et al., 2014).
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2015, Brain ResearchCitation Excerpt :Additionally, global synaptic scaling associated with spike-timing dependent regulation, the recent response history of populations of neurons, and behavioral relevance, also drive and adjust somatosensory cortical plasticity (Abbott and Nelson, 2000; Gambino and Holtmaat, 2012; Li et al., 2014). From a potentially therapeutic direction, short-term adaptation resulting from exposure to repeated peripheral mechanical stimuli has been shown to enhance intensity and frequency discrimination of supraliminal tactile stimuli (Lundstrom, 1986; Goble and Hollins, 1993, 1994), and improve spatial localization of subsequent stimuli (Tannan et al., 2006). Sustained adaptation can occur following prolonged stimulation (minutes, hours, days), resulting in changes of extracellular concentrations of ions (Franceschetti et al., 1995; Egelman and Montague, 1998), gene and protein expression (Polleux et al., 2007; Carulli et al., 2011; Vallès et al., 2011), and ultimately axonal sprouting and dendritic arborization which can modify regional connectivity (Lay et al., 2011; Freyer et al., 2012; Nudo and McNeal, 2013).