Foot sole skin vibration perceptual thresholds are elevated in a standing posture compared to sitting

doi:10.1016/j.gaitpost.2015.10.027

Gait & Posture

Volume 43, January 2016, Pages 87-92

https://doi.org/10.1016/j.gaitpost.2015.10.027 Get rights and content

Highlights

•
We measured skin vibration thresholds at the foot sole while standing and sitting.
•
Multiple frequencies were used to activate different cutaneous afferent populations.
•
Thresholds across all frequencies were increased during standing.

Abstract

Foot sole sensitivity is commonly assessed while individuals are seated or prone; however the primary role of foot sole cutaneous feedback is for the control of upright stance and gait. The aim of this study was to compare vibration perceptual thresholds across the foot sole between sitting and standing postures. Vibration perceptual thresholds were measured in sitting and standing postures in 18 healthy participants (8 male) using a custom vibration device. Two foot sole locations (heels and metatarsals) were tested at four vibration frequencies (3, 15, 40, and 250 Hz) selected to target different cutaneous afferent populations. At each frequency, perceptual thresholds across the foot sole were significantly higher in the standing posture compared to the sitting posture; this is indicative of lower sensitivity while standing. In addition, threshold differences between the heels and metatarsals for lower frequency vibratory stimuli were more pronounced while standing, with higher thresholds observed at the heels. Our results demonstrate that standing significantly alters sensitivity across the foot sole. Therefore, conducting perceptual tests at the foot sole during stance could potentially provide more direct information about the ability of cutaneous afferents to signal tactile information in a state where this feedback can contribute to postural control.

Introduction

Cutaneous afferents that innervate the foot sole signal information about pressure distribution under the feet as well as dynamic events such as slips and contact with the ground [1], [2]. This feedback plays an important role in the control of gait and posture [3], [4]. A decline in foot sole skin sensitivity occurs naturally with aging [5], [6] and as a result of neurological disorders, including Parkinson's disease and diabetic peripheral neuropathy [7], [8]. This decline in sensitivity is associated with poorer postural control and an increased risk of falls in these populations [6], [7], [8]. However, since sensory testing has been conducted exclusively with individuals seated or prone [5], [6], the natural ability of foot sole cutaneous afferents to signal dynamic events during stance remains unknown.

Cutaneous feedback is provided by four classes of cutaneous afferents that innervate the glabrous skin of the hands and feet. Each afferent class demonstrates unique adaptation and receptive field properties, and transmits specific features of tactile information. Fast adapting (FA) type I and type II afferents (innervating Meissner and Pacinian corpuscles, respectively) are sensitive to dynamic stimuli and their activation can evoke percepts of flutter and vibration [9], [10]. FA afferent feedback is thought to be responsible for signaling contact velocity and slips across the skin [1]. In contrast, slowly adapting (SA) type I and type II afferents (innervating Merkel discs and Ruffini endings, respectively) respond to sustained indentation and skin stretch and their activation can evoke percepts of pressure and movement at the skin [9], [10]. Recordings from single cutaneous afferents innervating the hand provide evidence that each afferent class is maximally responsive within a specific vibration frequency bandwidth; SA afferents to low frequencies (SAII <8 Hz, SAI 8–16 Hz) and FA afferents to higher frequencies (FAI 8–64 Hz and FAII >64 Hz) [11], [12], [13].

Vibration perceptual threshold (VPT) testing has been used to assess changes in skin sensitivity that occur with aging and neurological disorders [1], [5], [6], [7], [8]. VPT can be measured across different frequencies to allow for the function of the underlying cutaneous mechanoreceptors to be inferred. For example, older adults have been found to have higher VPTs at 50, 250 and 400 Hz [6] and at 25 and 100 Hz [5] compared to younger adults. This indicates a decline in cutaneous sensitivity across fast adapting cutaneous afferent classes, which is thought to contribute to observed impairments in postural control [5], [6].

To date, perceptual thresholds at the foot sole during stance, a position where skin feedback is of functional significance for the control of posture and gait, are unknown. The aim of this study was to compare VPT measured in a standing posture to VPT measured in a sitting posture at four frequencies designed to generate different cutaneous afferent population responses (3, 15, 40, and 250 Hz). Sustained pressure is known to cause adaptation in cutaneous afferents, which could make them less responsive to additional stimuli [14]. In addition, increased sensory feedback generated by movement and muscle contraction has been shown to gate the transmission of tactile sensory information to the primary somatosensory cortex [15], [16], [17]. Therefore, due to the load on the feet and increased postural demand during stance, it was hypothesized that threshold levels at the foot sole would be increased across all frequencies.

Section snippets

Participants

Eighteen healthy young adults aged, 22.2 ± 1.8 (8 males) participated in the study. Participants were free of neurological and musculoskeletal disorders. All participants provided written informed consent and all procedures were approved by the University of Guelph Research Ethics Board, which abides by the declaration of Helsinki.

Experimental setup

A custom device was developed to apply vibration to both foot soles during sitting and standing postures (Fig. 1A). This device consisted of a raised platform that

Results

Across all frequencies and both foot sole locations, VPT was higher in the standing posture compared to the sitting posture (Table 1, Fig. 2). Statistically, there were significant main effects of posture on VPT, indicating higher thresholds (lower sensitivity) while standing at all frequencies (3 Hz: F_(1,17) = 5.92, p = 0.0263; 15 Hz: F_(1,17) = 7.73, p = 0.0128; 40 Hz: F_(1,17) = 8.94, p = 0.0082; and 250 Hz: F_(1,17) = 7.51, p = 0.0140) (Fig. 2A). There were significant main effects of foot sole location on VPT

Discussion

Using a custom device, we were able to show that vibration perception thresholds (VPTs) at the heels and metatarsals were higher in a standing posture compared to a sitting posture. This finding could have implications for how skin information contributes functionally and perceptually while the feet are under loaded conditions while standing. Standing was found to increase VPTs across all four frequencies tested, indicating a general decrease in sensitivity across cutaneous afferent populations

Conflict of interest

These authors have no conflicts of interest to state regarding work presented in the current manuscript.

Acknowledgements

We would like to acknowledge Dan Rose and Steve Brown for their technical support. This work was supported by funding from the Natural Science and Engineering Research Council (NSERC) of Canada: NSERC Canada Graduate Scholarship (Masters) to R.L. Mildren, NSERC Postsecondary Graduate Scholarship (Doctoral) to N.D.J. Strzalkowski, and NSERC Discovery Grant to L.R. Bent (grant number 237924).

Author contributions: RLM was involved in conception and study design, data collection and analysis, and

References (30)

S.D. Perry
Evaluation of age-related plantar-surface insensitivity and onset age of advanced insensitivity in older adults using vibratory and touch sensation tests
Neurosci Lett
(2006)
B. Pratorius et al.
The sensitivity of the sole of the foot in patients with Morbus Parkinson
Neurosci Lett
(2003)
A.B. Vallbo
Sensations evoked from the glabrous skin of the human hand by electrical stimulation of unitary mechanosensitive afferents
Brain Res
(1981)
R.S. Johansson et al.
Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements
Brain Res
(1982)
S. Toma et al.
Response characteristics of cutaneous mechanoreceptors to vibratory stimuli in human glabrous skin
Neurosci Lett
(1995)
W. Jiang et al.
Modulation of cutaneous cortical evoked potentials during isometric and isotonic contractions in the monkey
Brain Res
(1990)
J.T. Inglis et al.
The role of cutaneous receptors in the foot
Adv Exp Med Biol
(2002)
M. Trulsson
Mechanoreceptive afferents in the human sural nerve
Exp Brain Res
(2001)
A. Kavounoudias et al.
Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation
J Physiol
(2001)
C. Maurer et al.
Human balance control during cutaneous stimulation of the plantar soles
Neurosi Lett
(2001)

C. Wells et al.

Regional variation and changes with ageing in vibrotactile sensitivity in the human footsole

J Gerontol A Biol Sci Med Sci

(2003)

L. Uccioli et al.

Body sway in diabetic neuropathy

Diabetes Care

(1995)

G. Macefield et al.

Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand

J Physiol

(1990)

W.H. Talbot et al.

The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand

J Neurophysiol

(1968)

Y.Y. Leung et al.

Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents

J Neurophysiol

(2005)

Cited by (36)

Postural performance and plantar cutaneous vibration perception in patients with idiopathic normal pressure hydrocephalus
2021, Heliyon
Citation Excerpt :
Since alterations of the force applied to the probe may affect tactile perception, force was controlled using a sensor (Hottinger U9B) [29]. An incremental forced-choice algorithm, modified after Mildren et al. [30], was implemented to automatically detect the VPT. Therefore, participants had to push a handheld trigger as soon as they perceived a vibration stimulus at the tested anatomical location.
To investigate whether impaired plantar cutaneous vibration perception contributes to postural disturbance in idiopathic normal pressure hydrocephalus (iNPH).
Three different groups were tested: iNPH-patients (iNPH), iNPH-patients after surgical shunt therapy (iNPH shunt), and healthy subjects (HS). Postural performance was quantified during quiescent stance on a pressure distribution platform. Vibration perception threshold (VPT) was measured using a modified vibration exciter to apply stimuli to the plantar foot.
Regarding postural performance, iNPH showed significantly higher values for all investigated center of pressure (COP)-parameters compared to HS, which suggests impaired postural control. Shunted patients presented a tendency towards better postural control in contrast to non-shunted patients. VPTs did not differ significantly between all investigated groups, which suggests comparable plantar cutaneous vibration perception.
Patients with iNPH suffer from poor postural stability, whereas shunting tends to affect postural performance positively. Plantar cutaneous vibration perception seems to be comparable between all investigated study groups. Consequently, postural disturbance in iNPH cannot clearly be ascribed to defective plantar cutaneous input.
A review of work environment risk factors influencing muscle fatigue
2020, International Journal of Industrial Ergonomics
Fatigue is a common and highly prevalent problem among workers. Muscle fatigue is the result of general fatigue that is caused due to demographical, physical, psychosocial, and environmental risk factors. This research was conducted to review the literature on the relationship between environmental risk factors and muscle fatigue. Forty papers that met the inclusion criteria were reviewed. Based on the review, Whole Body Vibration (WBV) and Local Vibration (LV) frequencies lower than 5 Hz and 20 Hz, respectively, cannot lead to muscle fatigue. In addition, the effect of WBV/LV magnitude on muscle fatigue is unclear. Furthermore, in a temperature below 19 °C and above 28 °C, a significant level of muscle fatigue can be expected. Moreover, surface electromyography is the most common tool for detecting the effect of environmental risk factors on muscle fatigue. The effect of simultaneous exposure to different environmental risk factors can be an interesting topic for future research.
To prevent musculoskeletal disorders, which are among the major challenge faced by employees and employers, is necessary to manage muscle fatigue. This manuscript explores environmental risk factors that can affect muscle fatigue.
Effects of water immersion on sensitivity and plantar skin properties
2018, Neuroscience Letters
Skin, as the largest organ of the human body, has various important functions, like protecting from dehydration or preventing the intrusion of microorganisms. Certain external factors have been shown to negatively influence skin functions. One of those factors is long-term (several hours) exposure to liquids, such as water, leading to skin softening. This study aimed to examine whether detrimental effects, such as skin softening, already exist after short-term water exposure. Furthermore, we investigated whether cutaneous sensation is altered by short-term water exposure. Thirty healthy subjects participated in this study (23.1 ± 2.5yrs, 173.7 ± 8.5 cm, 67.5 ± 9.8 kg). First, vibration perception thresholds (VPTs; 200 Hz), the skin´s elasticity (logarithmic decrement), and the skin´s mechanical deformation resistance properties (durometer readings) were measured at the plantar aspect of the hallux and heel of both feet (pre). Subsequently, one randomly chosen foot was immersed in water (45 min; water temperature adjusted to the foot pre temperatures). The contra-lateral foot remained untreated and out of the water. After the intervention, all three above-mentioned parameters were measured again in the same manner (post). Inferential statistical tests to detect differences regarding elasticity, durometer readings, and VPTs were performed based on logarithmically transformed data (natural logarithm). VPTs did not show significant differences. However, an overall increased elasticity and a softening effect of the skin were evident due to the water exposure at both anatomical locations. This study showed that 45 min of water exposure induces changes in plantar skin properties similar to the long-term effects described in other studies. Most importantly, the short-term water exposure resulted in a softening effect, which may affect skin perfusion in a negative manner. This may facilitate skin irritations and even future ulcer formation. We also showed that changes in mechanical skin properties induced by water exposure did not influence plantar cutaneous sensation. The findings of this study are especially relevant for people with impaired skin recovery mechanisms and highlight the importance of keeping skin dry, particularly in people who are bedridden.
Sensorimotor anatomy of gait, balance, and falls
2018, Handbook of Clinical Neurology
Citation Excerpt :
However, the sensitivity, perceptual thresholds, and sign of reflex responses (reflex reversal) evoked by activation of cutaneous receptors on the sole of the foot are critically dependent upon the state of vertical support (e.g., standing vs. sitting) and phase of locomotion (Duysens et al., 1990; De Serres et al., 1995). Thresholds are higher during quiet standing than during sitting (Mildren et al., 2016). Perceptual thresholds also differ across the sole of the foot, with lower thresholds in the ball and arch of the foot and higher thresholds in the regions of the heel and toe (Inglis et al., 2002).
The review demonstrates that control of posture and locomotion is provided by systems across the caudal-to-rostral extent of the neuraxis. A common feature of the neuroanatomic organization of the postural and locomotor control systems is the presence of key nodes for convergent input of multisensory feedback in conjunction with efferent copies of the motor command. These nodes include the vestibular and reticular nuclei and interneurons in the intermediate zone of the spinal cord (Rexed's laminae VI–VIII). This organization provides both spatial and temporal coordination of the various goals of the system and ensures that the large repertoire of voluntary movements is appropriately coupled to either anticipatory or reactive postural adjustments that ensure stability and provide the framework to support the intended action. Redundancies in the system allow adaptation and compensation when sensory modalities are impaired. These alterations in behavior are learned through reward- and error-based learning processes implemented through basal ganglia and cerebellar pathways respectively. However, neurodegenerative processes or lesions of these systems can greatly compromise the capacity to sufficiently adapt and sometimes leads to maladaptive changes that impair movement control. When these impairments occur, the risk of falls can be significantly increased and interventions are required to reduce morbidity.
Sensorimotor control of standing balance
2018, Handbook of Clinical Neurology
Citation Excerpt :
These properties may confer a role for FA afferents in coding transient balance-related movements (Kennedy and Inglis, 2002; Fallon et al., 2005). Note that loading of the feet while maintaining upright balance may increase the threshold of the foot sole afferents (Mildren et al., 2016), emphasizing that recordings from cutaneous afferents in a standing posture are critically needed to understand their role in balance. Afferents innervating joint receptors involved in somatosensation include low-threshold SA type I (Ruffini endings), low-threshold FA type II (Pacinian corpuscle), and high-threshold SA type III (Golgi-like receptors).
For most individuals, balancing upright is a simple task that requires little effort. The inherent difficulties associated with standing balance are not revealed until a pathology or injury impairs its control. Fundamentally, standing upright requires us to balance our unstable whole-body load within a small base of support. Small movements of the upright body are detected by various sensory receptors, all encoding these movements through their own coordinate system with specific dynamics. The balance controller filters, processes, and integrates sensory cues of body motion to produce an error signal between predicted and actual sensory consequences of balance-related movements. Compensatory motor commands are generated in response to this error to maintain upright standing. In the present review, we first briefly describe the biomechanics and sensor dynamics of standing balance. We further review sensorimotor and perceptual approaches revealing operational principles of the balance system, along with computational approaches that explore control processes underlying upright stance. Finally, we present robotic tools that virtualize the sensory consequences, biomechanics, and/or environmental factors inherent to the standing balance task. Throughout, we emphasize works that combine sensorimotor, computational, and/or robotics approaches to highlight the task dependency, multisensory cue combinations, cortical-subcortical contributions, and internal representations underpinning balance control.
Subliminal electrical and mechanical stimulation does not improve foot sensitivity in healthy elderly subjects
2018, Clinical Neurophysiology Practice
Citation Excerpt :
Since sensory data are recorded on a ratio scale, they lead to heteroscedastic errors (Nevill and Atkinson, 1997). To correct heteroscedasticity and the non-normality distribution, data were transformed with the natural logarithm (Mildren et al., 2015; Nevill and Atkinson, 1997). While the heteroscedasticity could be eliminated, not all parameters were distributed normally after transformation.
Deterioration of cutaneous perception may be one reason for the increased rate of falling in the elderly. The stochastic resonance phenomenon may compensate this loss of information by improving the capability to detect and transfer weak signals. In the present study, we hypothesize that subliminal electrical and mechanical noise applied to the sole of the foot of healthy elderly subjects improves vibration perception thresholds (VPT).
VPTs of 99 healthy elderly subjects were measured at 30 Hz at the heel and first metatarsal head (MET I). Participants were randomly assigned to one of five groups: vibration (Vi-G), current (Cu-G), control (Co-G), placebo-vibration (Pl-Vi), and placebo-current (Pl-Cu). Vi-G and Cu-G were stimulated using 90% (subliminal) of their individual perception thresholds for five minutes in a standing position. Co-G received no stimulation. The placebo groups were treated with mock stimulation. VPTs were measured twice before the intervention (baseline (BASE) and pre-measurement (PRE)), and once after the intervention (post-measurement (POST)).
Significant differences were found between measurement conditions comparing BASE and POST, and PRE and POST. VPTs between groups within each measurement condition showed no significant differences. Vi-G was the only group that showed significantly higher VPTs in POST compared to BASE and PRE, which contradicts previous studies.
We analyzed increased VPTs after subliminal mechanical stimulation. The pressure load of standing for five minutes combined with subliminal stimulation may have shifted the initial level of mechanoreceptor sensitivity, which may lead to a deterioration of the VPT. The subliminal electrical stimulation had no effect on VPT.
Based on our results, we cannot confirm positive effects of subliminal electrical or mechanical stimulation on the sole of the foot.

View all citing articles on Scopus

View full text

Foot sole skin vibration perceptual thresholds are elevated in a standing posture compared to sitting

Highlights

Abstract

Introduction

Section snippets

Participants

Experimental setup

Results

Discussion

Conflict of interest

Acknowledgements

Neurosci Lett

Neurosci Lett

Brain Res

Brain Res

Neurosci Lett

Brain Res

The role of cutaneous receptors in the foot

Adv Exp Med Biol

Mechanoreceptive afferents in the human sural nerve

Exp Brain Res

Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation

J Physiol

Human balance control during cutaneous stimulation of the plantar soles

Neurosi Lett

Regional variation and changes with ageing in vibrotactile sensitivity in the human footsole

J Gerontol A Biol Sci Med Sci

Body sway in diabetic neuropathy

Diabetes Care

Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand

J Physiol

The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand

J Neurophysiol

Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents

J Neurophysiol