Edited by: Juergen Konczak, University of Minnesota, USA
Reviewed by: Thomas Weiss, Friedrich Schiller University Jena, Germany; Ann Van De Winckel, University of Minnesota, USA
This article was submitted to the journal Frontiers in Human Neuroscience.
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Hand motor impairment persists after stroke. Sensory inputs may facilitate recovery of motor function. This pilot study tested the effectiveness of tactile sensory noise in improving hand motor function in chronic stroke survivors with tactile sensory deficits, using a repeated measures design. Sensory noise in the form of subthreshold, white noise, mechanical vibration was applied to the wrist skin during motor tasks. Hand dexterity assessed by the Nine Hole Peg Test and the Box and Block Test and pinch strength significantly improved when the sensory noise was turned on compared with when it was turned off in chronic stroke survivors. The subthreshold sensory noise to the wrist appears to induce improvements in hand motor function possibly via neuronal connections in the sensoriomotor cortex. The approach of applying concomitant, unperceivable mechanical vibration to the wrist during hand motor tasks is easily adoptable for clinic use as well as unsupervised home use. This pilot study suggests a potential for a wristband-type assistive device to complement hand rehabilitation for stroke survivors with sensorimotor deficit.
Many strokes survivors suffer from persistent hand impairment (Wade et al.,
Post-stroke somatosensory deficits are quite prevalent (Carey,
The need for intact sensory input preceding motor rehabilitation is clear. As such, a few methods to influence the sensory system have been developed. They include sensory discrimination training, passive sensory stimulation, temporary deafferentation, and sensory noise. Sensory discrimination training involves patients’ repeated practice to distinguish textures, localize tactile stimulus, and detect body positions (Carey and Matyas,
The sensory noise method involves application of a small level of mechanical vibration to the skin to result in immediate improvement in sensorimotor function (Collins et al.,
Application of noise to the forearm, although not directly to the hand, has also been shown to improve hand sensorimotor function by shortening reaction time to hand tactile stimuli in healthy adults (Hur et al.,
While presenting great potential to meet the need of stroke survivors with sensorimotor deficits in the hand, application of subthreshold vibrotactile noise off the hand has not been examined for its efficacy in improving stroke survivors’ hand motor function and dexterity. The objective of this study was to evaluate the effectiveness of subthreshold vibrotactile noise applied to the wrist in improving hand motor function for stroke survivors with tactile sensory deficits. The hypothesis was that use of subthreshold vibrotactile noise at the wrist would enhance hand motor function in stroke survivors. In particular, hand dexterity and maximum pinch grip strength were hypothesized to improve with the sensory noise, because sensory feedback is critical for dexterous hand movement (Johansson and Westling,
Ten chronic stroke survivors (>6 months post stroke) with tactile sensory deficits were recruited for this study. Stroke survivors with a Semmes-Weinstein monofilament score >2.83 on either the thumb tip or the index fingertip were defined as having tactile sensory deficits (Cooper and Canyock,
Subject | Age | Gender | Paretic hand | Time since stroke (years) | Chedoke (/7) | Fugl-Meyer (/24) |
---|---|---|---|---|---|---|
V01 | 62 | M | Left | 14 | 7 | 22 |
V02 | 62 | M | Left | 7 | 6 | 16 |
V03 | 63 | F | Left | 10 | 5 | 16 |
V04 | 53 | F | Left | 5 | 7 | 24 |
V05 | 68 | F | Left | 9 | 2 | 2 |
V06 | 60 | M | Left | 9 | 5 | 22 |
V07 | 56 | M | Right | 5 | 6 | 14 |
V08 | 82 | M | Right | 2 | 6 | 23 |
V09 | 67 | M | Left | 2 | 7 | 24 |
V10 | 61 | M | Right | 12 | 7 | 24 |
Stroke survivors’ paretic hand motor function was compared with and without subthreshold vibrotactile noise to the wrist. A set of hand function tests was repeated in four blocks, without noise for blocks one and four and with noise for blocks two and three. Learning effects were accounted by providing a practice block prior to data collection.
Vibrotactile noise was applied using two C-3 tactors (Engineering Acoustics, Inc., Casselberry, FL, USA) attached to the volar and dorsal wrist of the paretic arm using adhesive tapes (Figure
Hand dexterity and pinch grip strength constituted the main outcome measures for the hand motor function. Hand manual dexterity was assessed using the Nine Hole Peg Test (NHPT) and the Box and Block Test (BBT) (Figures
In addition to the hand motor function, wrist motor function was assessed using the active range of motion (ROM), in case the increased motor output with the sensory noise to the wrist extends beyond the hand. The active ROM of the wrist was measured using a digital goniometer while the subject voluntarily and maximally flexed and extended their wrist. To replicate the previous finding of finger sensory enhancement with the vibrotactile noise to the wrist (Enders et al.,
For the main analysis, the Kruskal–Wallis test was used on the multivariate data to test if the noise (with vs. without) significantly affected the main outcome measures – the NHPT time, BBT score, and pinch grip strength. For the secondary analysis, three additional Kruskal–Wallis tests were performed to examine the effect of noise on the grip force deviation, the wrist ROM and the monofilament score, separately. In addition, responsiveness of the individual main outcome measures to the noise intervention and correlations among the noise-induced changes in the three main outcome measures were examined using the standardized response means (Cohen,
Subthreshold vibrotactile noise to the wrist significantly improved stroke survivors’ hand dexterity and strength (
In this pilot study, remote sensory noise enhanced the hand motor function for chronic stroke survivors with tactile sensory deficits, as seen by improved NHPT, BBT, and maximum pinch grip strength with subthreshold vibrotactile noise applied to the wrist. Moderate responsiveness was observed for all three main outcome measures. These improvements support the hypothesis that remote sensory noise facilitates hand dexterity and strength. While facilitating dexterity and maximum pinch grip strength, the remote sensory noise did not appear to affect the active ROM of the wrist, suggesting that the wrist sensory noise influenced coordination and activation of muscles located within the hand, but not those of the forearm muscles. Such specificity may suggest involvement of direct connections between the somatosensory and motor cortices (Jones et al.,
Contrary to the previous study (Enders et al.,
A number of previous studies have also shown motor improvement immediately following application of sensory noise or sensory stimulation not only in healthy adults but also in stroke survivors with motor deficits (Priplata et al.,
The present study applied sensory noise simultaneously with targeted motor tasks to induce improvement in hand dexterity and strength. The use of noise during targeted motor tasks for instant effects differentiates this method from others that apply sensory stimulation for up to 2 h at a time to prime the sensory system prior to targeted motor tasks (Tegenthoff et al.,
The present method used subthreshold sensory noise to induce improvement in hand dexterity and strength. It is different from other techniques that used suprathreshold sensory stimulation, sometimes strong enough to cause paresthesia (Conforto et al.,
White noise was used in the present study. As opposed to constant frequency stimulation, white noise may reduce sensory adaptation and enhance the effect of sensory stimulation (McDonnell and Abbott,
The last unique feature of this study is that the sensory noise was applied to the wrist, with resulting improvements in hand dexterity and strength. Spreading effects of sensory manipulation have been shown in the past. For instance, subthreshold vibrotactile noise to the wrist resulted in improved touch sensation on the fingers in stroke survivors (Enders et al.,
The focus of stroke rehabilitation is to regain or improve function. For stroke survivors, improving function could mean an increased ability to perform activities of daily living. Manual dexterity has been shown to be indicative of functional independence. Noise-induced improvements seen in reliable measures such as the NHPT, BBT, and hand strength in this pilot study indicate the possibility of increased functional independence.
The features of our approach enable the potentially easy adoption of subthreshold sensory noise for home or clinic use. Our approach applied an unperceivable, minute level of vibration to the wrist, concomitantly during targeted motor tasks, with instant effects on hand motor function. Simple mechanical vibration can be produced with low-cost devices and fewer safety concerns, compared with deafferentation via anesthesia, constant current electrical stimulation, or transcranial magnetic stimulation, which are not readily accessible and have greater safety risks. Unperceivable, minute vibration does not cause discomfort, pain, or paresthesia, and is thus more patient-friendly. Application of noise to the wrist, as opposed to the fingers (Liu et al.,
The improvements reported in this pilot study may be small, although they are statistically significant. These improvements were obtained instantaneously, and repeated use with therapy may result in greater clinical impact by allowing practices in sensorimotor integration and providing intensity needed for recovery (Kwakkel,
Use of this approach during therapy may be designed with consideration of possible sensory adaptation. Therapy with continuous noise longer than 15–20 min may not yield additional benefits of using the noise to improve sensory perception. Thus a few minute break may be taken before continuing another round of therapy for 15–20 min to recover from sensory adaptation (Berglund and Berglund,
In this pilot study, hand dexterity and strength improved with subthreshold vibrotactile noise at the wrist in chronic stroke survivors with tactile sensory deficits. The noise-induced improvements in hand motor function may have been mediated by cortical interneuronal connections from the wrist somatosensory area to the finger motor area. The approach of applying concomitant, unperceivable mechanical vibration to the wrist during hand motor tasks is easily adoptable for clinic use as well as unsupervised home use. This pilot study suggests the potential for developing an assistive device worn at the wrist, applying subthreshold vibrotactile noise to enhance hand motor function. Such a device would be placed remotely from the fingers and palm so as not to interfere with object manipulation or dexterous hand function and to allow the hand to receive relevant tactile stimuli. Such an assistive device or sensory orthosis may complement hand rehabilitation for patients with stroke with sensorimotor deficit, and thus, lead to increased functional independence and enhanced quality of life.
There is a pending patent for a wearable device for improving tactile sensitivity, involving use of the sensory noise, similarly with the present manuscript. Na Jin Seo and Leah R. Enders are listed as inventors of this pending patent.
This project was partially supported by the American Heart Association, the University of Wisconsin–Milwaukee, and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant Number 8UL1TR000055. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. The authors would like to thank Dr. Rodney Sparapani in the Division of Biostatistics at the Medical College of Wisconsin for his consultation on statistical analysis and Jeff King at the University of Wisconsin–Milwaukee for his editorial service.