Somatosensory &M otor Research
http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic)
informa
Somatosens M o t Res, 2015; 32(1): 4 4 -5 0
healthcare
© 2015 Inform a UK Ltd. DOI: 10.3109/08990220.2014.958216
ORIGINAL ARTICLE
Age- and sex-related changes in vibrotactile sensitivity of hand and face in neurotypical adults Lalit Venkatesan1, Steven M. Barlow1,2,3,4, & Douglas Kieweg5 ’Communication Neuroscience Laboratories, University of Nebraska, Lincoln, NE, USA, 2Department o f Special Education and Communication Disorders, University o f Nebraska, Lincoln, NE, USA, 3Center for Brain, Biology and Behavior, University o f Nebraska, Lincoln, NE, USA, 4Department of Biological Systems Engineering, University o f Nebraska, Lincoln, NE, USA, and 5Department o f Mechanical Engineering, University o f Kansas, Lawrence, KS, USA
A b s tra c t
K e y w o rd s
Sensory perception decreases with age, and is altered as a function o f sex. Very little is known about the age- and sex-related changes in vibrotactile detection thresholds (VDTs) of the face relative to the glabrous hand. This study utilized a single-interval up/down (SIUD) adaptive procedure to estimate the VDT for mechanical stimuli presented at 5, 10, 50, 150, 250, and 300 Hz at tw o sites on the face, including the right non-glabrous surface of the oral angle and the right lower lip vermilion; and on the hand on the glabrous surface o f the distal phalanx of the right dominant index finger. Eighteen right-handed healthy younger adults and 18 righthanded healthy older adults participated in this study. VDTs were significantly different between the three stimulus sites ( p < 0.0001), and dependent on stimulus frequency ( p < 0.0001) and the sex o f the participants ( p < 0.005). VDTs were significantly higher for older adults when compared to younger adults for the finger stimulation condition (p < 0.05). There were significant differences ( p < 0.05) in cheek and lower lip VDTs between male and female subjects. Difference in the VDTs between the three stimulation sites is presumed to reflect the unique typing and distribution o f mechanoreceptors in the face and hand. Agerelated differences in finger skin sensitivity are likely due to changes in the physical structure of skin, changes in the number and morphology o f the mechanoreceptors, differences in the functional use o f the hand, and its central representation. Sex-related differences in the VDTs may be due to the differences in tissue conformation and thickness, mechanoreceptor densities, skin hydration, or temperature characteristics.
Aging, automatic adaptive threshold tracking, glabrous, non-glabrous, sensory
Introduction The differences in the vibrotactile threshold sensitivities of the hand (Verrillo 1979a, 1979b, 1980, 1982, 1983; Barlow 1987) and face (Verrillo and Ecker 1977; Barlow 1987) have been studied extensively for well over 30 years. The lower face is characterized by the prevalence of SA (slow adapting) mechanoreceptive units with high dynamic sensitivity and irregular discharge during sustained tissue deformation, which resemble the SA I units in the hairy and glabrous skin of the human hand (Johansson et al. 1988). FA (fast adapting) units are very common in both the hairy and glabrous skin of the hand, but are less prevalent in the face. Properties of the few FA units observed in the face were similar to the FA I units found in the hand (Johansson et al. 1988). However, the classic Pacinian response present in the glabrous hand for vibratory Correspondence: S. M. Barlow, Corwin Moore Professor, Department of Special Education and Communication Disorders, University of Nebraska, 272 Barkley Memorial Center, Lincoln, NE 68583, USA. Tel: +1 402 472 6395. Fax: +1 402 472 7697. E-mail: [email protected]
H is to r y
Received 30 April 2014 Revised 20 June 2014 Accepted 5 August 2014 Published online 24 September 2014
input at 250 Hz is absent in hairy and glabrous perioral areas (Barlow 1987; Johansson et al. 1988; Nordin and Hagbarth 1989). Apart from the mechanoreceptor typing, histochemical and morphological analyses revealed an apparent lack of muscle spindle receptors and Golgi tendon organs in the face (Stal et al. 1987, 1990). Facial muscle fibers insert directly into the skin rather than the connective tissue making it possible for embedded mechanoreceptors to encode information about changes in muscle length and force. Pseudo-Ruffini endings (Nordin and Hagbarth 1989) may serve some of the function ality to encode facial proprioception (Barlow 1987, 1998). A number of studies have illustrated changes in vibrotactile sensitivity of the hand as a function of age, and the loss of sensitivity is pronounced at the frequencies (80-250 Hz) that activate the Pacinian corpuscles (Verrillo 1993; Gescheider et al. 1994, 2004). The density of Pacinian corpuscles in the deep part of the human palmar corium, palmar subcutaneous tissue, and at the sides of the middle and proximal phalanges adjacent to the periosteum decreases with age (Cauna 1965). Female fingers have higher densities of Meissner’s corpuscles (Dillon et al. 2001) and Merkel disks (Peters et al. 2009) when
DOl: 10.3109/08990220.20J 4.958216
compared to males. A significant decrease in the concentra tion of Meissner’s corpuscles (Bruce 1980; Iwasaki et al. 2003) was observed in the distal phalanges, and these changes were correlated to age. Psychophysical studies exploring the influence of age and sex on the perception of vibratory stimuli applied to the glabrous surface of the hand showed that vibrotactile detection thresholds (VDTs) significantly increased as a function of age, and a larger rate of threshold increase was noted in both male and female subjects beyond 65-70 years of age. Sex-based differences in vibrotactile sensitivity were not significant between the younger male and female subjects, but older female subjects had significantly lower thresholds when compared to older male subjects (Verrillo 1979b; Gescheider et al. 1994). Although significant effects of aging were observed among the four types of A/3 mechanoreceptors, the aging effect was more prominent in the Pacinian corpuscle frequency response (Verrillo 1979a; Gescheider et al. 1994). Anatomical and morphological differences between the hand and face are evident, and vibrotactile perception of the hand is altered as a function of age and sex. However, there is limited evidence on how age and sex influence the VDTs of the face. This information would be useful for determining the prognosis or designing treatments for neurological insults (e.g., cerebral stroke) or diseases common in older adults (Wohlert and Smith 1998). We addressed this issue by utilizing a recently established psychophysical protocol to study age- and sex-related changes in facial vibrotactile sensitivity and compared it to the hand. Vibrotactile sensitivity thresholds were determined for different stimulus frequencies (5, 10, 50, 150, 250, and 300 Hz) at two sites on the face (right lower lip vermilion and right non-glabrous surface of oral angle) and one site on the hand (index finger) in neurotypical adults. The influence of age and sex, and the interaction of these independent variables on vibrotactile sensitivity was compared between the three skin sites described above. Materials and methods Participants
Eighteen neurotypical younger adults (9M [24.44 (SD = 2.27) years] and 9F [23.11 (S D = 1.93) years]) and 18 neurotypical older adults (9M [64.78 (SD = 3.13) years] and 9F [63.67 (SD = 3.11) years]) were recruited regardless of race or ethnicity. Written informed consent, approved by the University Institutional Review Board, was obtained for each participant. Participants were compensated for their participation in this study. Inclusion criteria: right-handed according to the Edinburgh handedness scale (Oldfield 1971) with no report of neurological or psychiatric illness, and not taking regular medication. Exclusion criteria: neurological, sensory and/or muscular deficits, psychiatric abnormalities, or with abnormal skin sensitivity on face or hand. Vibrotactile detection threshold (VDT) assessment for hand and face
Stimulus control An established psychophysical stimulus generation system was used to assess cutaneous vibrotactile sensitivity in the
Human vibrotactile sensitivity
45
lower face and hand (Barlow 1987; Andreatta and Barlow 2003, 2009; Andreatta et al. 2003; Andreatta and Davidow 2006). A National Instruments cRIO real-time embedded controller was programmed in LabVIEW to synthesize (NI 9263, 16 bit, lOOKS/s) sinusoidal bursts that were Is in duration with a 100 ms linear rise-fall decay to circum vent mechanical transients. This signal was conditioned by a Briiel & Kjaer model 2706 power amplifier and input to a Briiel & Kjaer model 4810 Minishaker. The Minishaker includes custom fixtures and sensors for precision vibrotac tile stimulation and measurement, a stainless steel shaft and nylon contactor probe (area = 0.5 cm2), and a stainless steel rigid surround (annular gap at 1 mm) coupled to a linear translation stage with integral micrometer (for calibration and tissue preload). This configuration allows the surface of the rigid surround to be adjusted relative to the contactor probe to produce a 1000 pm tissue preload against the moving stimulator probe. A Schaevitz micro miniature displacement sensor provided an output signal linearly related to contactor probe displacement from DC to 800 Hz (resolution 0.01 pm). Participants were seated in a dental examination chair with an articulating headrest, and asked to press a response button when they detected the vibratory stimulus. A double adhesive collar (7/16" ID) was placed on the stainless steel surround of the Briiel & Kjaer Minishaker to secure placement of the probe on the target skin site. Adaptive vibrotactile threshold tracking algorithm A single-interval up/down (SIUD) adaptive procedure based on eight trials was used to estimate vibrotactile thresholds (Lecluyse and Meddis 2009) for stimuli presented at 5, 10, 50, 150, 250, and 300 Hz on the glabrous surface of the distal phalanx of the right dominant index finger (Figure 1(a)), and at two sites on the face, including the right non-glabrous surface of the oral angle (Figure 1(b)) and the right lower lip vermilion (Figure 1(c)). These sinusoidal vibrotactile inputs correspond well to the frequency sensitivity of cutaneous mechanoreceptors innervating the face and hand. Test order for site and stimulus frequency was randomized among participants. Participants wore circumaural headphones with narrow-band noise plus a pure tone centered at the active test frequency (5, 10, 50, 150, 250, or 300 Hz) to mask the potential acoustic emittance associated with the Minishaker in the audio range (>50Hz). The SIUD procedure used in this study for measuring absolute VDT is based on the subject response during stimulus presentation. Subjects were requested to press a response button when they perceived the vibratory stimulus. A detailed description of the SIUD algorithm is available in the article published by Lecluyse and Meddis (2009). We briefly describe our adaptation of the algorithm below. In accordance with the procedure described by Lecluyse and Meddis (2009), the initial stimulus amplitude was set at a supra-threshold level in order to guarantee a response. The initial step size was set at 10 dB and then randomly varied in a ±5dB range relative to the initial amplitude. After the first negative response, the stimulus level was set at the mid-point between the previous two levels, and a 2 dB step was utilized.
46
Somatosens Mot Res, 2015; 32(1): 44-50
L. Venkatesan et al.
Figure 1. Positioning of the vibrotactile stimulator (modified Briiel & Kjaer 4810 Minishaker) for (a) index finger, (b) cheek, and (c) lower lip vermilion stimulation.
VDT testing continued for eight trials starting from the trial prior to the first negative response. The algorithm imple mented in this study used false positive detection tests in which no vibrotactile stimulus was presented, but the participant was expected to respond. These false positive trials were implemented in 20% of the successive trials, and on detection of a false positive trial, it was discarded and a new trial was restarted. The number of trials (n = 8) included in threshold estimation was chosen in order to attain an accuracy of ±2 dB and this number excludes the false positive trials. As per the S1UD algorithm, a required accuracy of ±1 dB would entail the use of 26 non-false positive trials. In this study, we estimated the VDTs for six different frequencies in three different stimulation sites (n = 18), and in order to reduce the strain on the subjects we concluded that an accuracy of ±2 dB is adequate. S t a t is t ic a l a n a ly s is
A repeated measures ANOVA was performed using Minitab’' statistics software (version 16). A mixed-model was utilized to assess the dependence of VDTs on age and sex (between subjects), and stimulation frequency and site (within subjects).
Results
The statistical analysis revealed VDTs were significantly dependent on stimulus site (F = 132.99, p < 0.0001), fre quency of stimulation (F = 128.98,/?
http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic)
informa
Somatosens M o t Res, 2015; 32(1): 4 4 -5 0
healthcare
© 2015 Inform a UK Ltd. DOI: 10.3109/08990220.2014.958216
ORIGINAL ARTICLE
Age- and sex-related changes in vibrotactile sensitivity of hand and face in neurotypical adults Lalit Venkatesan1, Steven M. Barlow1,2,3,4, & Douglas Kieweg5 ’Communication Neuroscience Laboratories, University of Nebraska, Lincoln, NE, USA, 2Department o f Special Education and Communication Disorders, University o f Nebraska, Lincoln, NE, USA, 3Center for Brain, Biology and Behavior, University o f Nebraska, Lincoln, NE, USA, 4Department of Biological Systems Engineering, University o f Nebraska, Lincoln, NE, USA, and 5Department o f Mechanical Engineering, University o f Kansas, Lawrence, KS, USA
A b s tra c t
K e y w o rd s
Sensory perception decreases with age, and is altered as a function o f sex. Very little is known about the age- and sex-related changes in vibrotactile detection thresholds (VDTs) of the face relative to the glabrous hand. This study utilized a single-interval up/down (SIUD) adaptive procedure to estimate the VDT for mechanical stimuli presented at 5, 10, 50, 150, 250, and 300 Hz at tw o sites on the face, including the right non-glabrous surface of the oral angle and the right lower lip vermilion; and on the hand on the glabrous surface o f the distal phalanx of the right dominant index finger. Eighteen right-handed healthy younger adults and 18 righthanded healthy older adults participated in this study. VDTs were significantly different between the three stimulus sites ( p < 0.0001), and dependent on stimulus frequency ( p < 0.0001) and the sex o f the participants ( p < 0.005). VDTs were significantly higher for older adults when compared to younger adults for the finger stimulation condition (p < 0.05). There were significant differences ( p < 0.05) in cheek and lower lip VDTs between male and female subjects. Difference in the VDTs between the three stimulation sites is presumed to reflect the unique typing and distribution o f mechanoreceptors in the face and hand. Agerelated differences in finger skin sensitivity are likely due to changes in the physical structure of skin, changes in the number and morphology o f the mechanoreceptors, differences in the functional use o f the hand, and its central representation. Sex-related differences in the VDTs may be due to the differences in tissue conformation and thickness, mechanoreceptor densities, skin hydration, or temperature characteristics.
Aging, automatic adaptive threshold tracking, glabrous, non-glabrous, sensory
Introduction The differences in the vibrotactile threshold sensitivities of the hand (Verrillo 1979a, 1979b, 1980, 1982, 1983; Barlow 1987) and face (Verrillo and Ecker 1977; Barlow 1987) have been studied extensively for well over 30 years. The lower face is characterized by the prevalence of SA (slow adapting) mechanoreceptive units with high dynamic sensitivity and irregular discharge during sustained tissue deformation, which resemble the SA I units in the hairy and glabrous skin of the human hand (Johansson et al. 1988). FA (fast adapting) units are very common in both the hairy and glabrous skin of the hand, but are less prevalent in the face. Properties of the few FA units observed in the face were similar to the FA I units found in the hand (Johansson et al. 1988). However, the classic Pacinian response present in the glabrous hand for vibratory Correspondence: S. M. Barlow, Corwin Moore Professor, Department of Special Education and Communication Disorders, University of Nebraska, 272 Barkley Memorial Center, Lincoln, NE 68583, USA. Tel: +1 402 472 6395. Fax: +1 402 472 7697. E-mail: [email protected]
H is to r y
Received 30 April 2014 Revised 20 June 2014 Accepted 5 August 2014 Published online 24 September 2014
input at 250 Hz is absent in hairy and glabrous perioral areas (Barlow 1987; Johansson et al. 1988; Nordin and Hagbarth 1989). Apart from the mechanoreceptor typing, histochemical and morphological analyses revealed an apparent lack of muscle spindle receptors and Golgi tendon organs in the face (Stal et al. 1987, 1990). Facial muscle fibers insert directly into the skin rather than the connective tissue making it possible for embedded mechanoreceptors to encode information about changes in muscle length and force. Pseudo-Ruffini endings (Nordin and Hagbarth 1989) may serve some of the function ality to encode facial proprioception (Barlow 1987, 1998). A number of studies have illustrated changes in vibrotactile sensitivity of the hand as a function of age, and the loss of sensitivity is pronounced at the frequencies (80-250 Hz) that activate the Pacinian corpuscles (Verrillo 1993; Gescheider et al. 1994, 2004). The density of Pacinian corpuscles in the deep part of the human palmar corium, palmar subcutaneous tissue, and at the sides of the middle and proximal phalanges adjacent to the periosteum decreases with age (Cauna 1965). Female fingers have higher densities of Meissner’s corpuscles (Dillon et al. 2001) and Merkel disks (Peters et al. 2009) when
DOl: 10.3109/08990220.20J 4.958216
compared to males. A significant decrease in the concentra tion of Meissner’s corpuscles (Bruce 1980; Iwasaki et al. 2003) was observed in the distal phalanges, and these changes were correlated to age. Psychophysical studies exploring the influence of age and sex on the perception of vibratory stimuli applied to the glabrous surface of the hand showed that vibrotactile detection thresholds (VDTs) significantly increased as a function of age, and a larger rate of threshold increase was noted in both male and female subjects beyond 65-70 years of age. Sex-based differences in vibrotactile sensitivity were not significant between the younger male and female subjects, but older female subjects had significantly lower thresholds when compared to older male subjects (Verrillo 1979b; Gescheider et al. 1994). Although significant effects of aging were observed among the four types of A/3 mechanoreceptors, the aging effect was more prominent in the Pacinian corpuscle frequency response (Verrillo 1979a; Gescheider et al. 1994). Anatomical and morphological differences between the hand and face are evident, and vibrotactile perception of the hand is altered as a function of age and sex. However, there is limited evidence on how age and sex influence the VDTs of the face. This information would be useful for determining the prognosis or designing treatments for neurological insults (e.g., cerebral stroke) or diseases common in older adults (Wohlert and Smith 1998). We addressed this issue by utilizing a recently established psychophysical protocol to study age- and sex-related changes in facial vibrotactile sensitivity and compared it to the hand. Vibrotactile sensitivity thresholds were determined for different stimulus frequencies (5, 10, 50, 150, 250, and 300 Hz) at two sites on the face (right lower lip vermilion and right non-glabrous surface of oral angle) and one site on the hand (index finger) in neurotypical adults. The influence of age and sex, and the interaction of these independent variables on vibrotactile sensitivity was compared between the three skin sites described above. Materials and methods Participants
Eighteen neurotypical younger adults (9M [24.44 (SD = 2.27) years] and 9F [23.11 (S D = 1.93) years]) and 18 neurotypical older adults (9M [64.78 (SD = 3.13) years] and 9F [63.67 (SD = 3.11) years]) were recruited regardless of race or ethnicity. Written informed consent, approved by the University Institutional Review Board, was obtained for each participant. Participants were compensated for their participation in this study. Inclusion criteria: right-handed according to the Edinburgh handedness scale (Oldfield 1971) with no report of neurological or psychiatric illness, and not taking regular medication. Exclusion criteria: neurological, sensory and/or muscular deficits, psychiatric abnormalities, or with abnormal skin sensitivity on face or hand. Vibrotactile detection threshold (VDT) assessment for hand and face
Stimulus control An established psychophysical stimulus generation system was used to assess cutaneous vibrotactile sensitivity in the
Human vibrotactile sensitivity
45
lower face and hand (Barlow 1987; Andreatta and Barlow 2003, 2009; Andreatta et al. 2003; Andreatta and Davidow 2006). A National Instruments cRIO real-time embedded controller was programmed in LabVIEW to synthesize (NI 9263, 16 bit, lOOKS/s) sinusoidal bursts that were Is in duration with a 100 ms linear rise-fall decay to circum vent mechanical transients. This signal was conditioned by a Briiel & Kjaer model 2706 power amplifier and input to a Briiel & Kjaer model 4810 Minishaker. The Minishaker includes custom fixtures and sensors for precision vibrotac tile stimulation and measurement, a stainless steel shaft and nylon contactor probe (area = 0.5 cm2), and a stainless steel rigid surround (annular gap at 1 mm) coupled to a linear translation stage with integral micrometer (for calibration and tissue preload). This configuration allows the surface of the rigid surround to be adjusted relative to the contactor probe to produce a 1000 pm tissue preload against the moving stimulator probe. A Schaevitz micro miniature displacement sensor provided an output signal linearly related to contactor probe displacement from DC to 800 Hz (resolution 0.01 pm). Participants were seated in a dental examination chair with an articulating headrest, and asked to press a response button when they detected the vibratory stimulus. A double adhesive collar (7/16" ID) was placed on the stainless steel surround of the Briiel & Kjaer Minishaker to secure placement of the probe on the target skin site. Adaptive vibrotactile threshold tracking algorithm A single-interval up/down (SIUD) adaptive procedure based on eight trials was used to estimate vibrotactile thresholds (Lecluyse and Meddis 2009) for stimuli presented at 5, 10, 50, 150, 250, and 300 Hz on the glabrous surface of the distal phalanx of the right dominant index finger (Figure 1(a)), and at two sites on the face, including the right non-glabrous surface of the oral angle (Figure 1(b)) and the right lower lip vermilion (Figure 1(c)). These sinusoidal vibrotactile inputs correspond well to the frequency sensitivity of cutaneous mechanoreceptors innervating the face and hand. Test order for site and stimulus frequency was randomized among participants. Participants wore circumaural headphones with narrow-band noise plus a pure tone centered at the active test frequency (5, 10, 50, 150, 250, or 300 Hz) to mask the potential acoustic emittance associated with the Minishaker in the audio range (>50Hz). The SIUD procedure used in this study for measuring absolute VDT is based on the subject response during stimulus presentation. Subjects were requested to press a response button when they perceived the vibratory stimulus. A detailed description of the SIUD algorithm is available in the article published by Lecluyse and Meddis (2009). We briefly describe our adaptation of the algorithm below. In accordance with the procedure described by Lecluyse and Meddis (2009), the initial stimulus amplitude was set at a supra-threshold level in order to guarantee a response. The initial step size was set at 10 dB and then randomly varied in a ±5dB range relative to the initial amplitude. After the first negative response, the stimulus level was set at the mid-point between the previous two levels, and a 2 dB step was utilized.
46
Somatosens Mot Res, 2015; 32(1): 44-50
L. Venkatesan et al.
Figure 1. Positioning of the vibrotactile stimulator (modified Briiel & Kjaer 4810 Minishaker) for (a) index finger, (b) cheek, and (c) lower lip vermilion stimulation.
VDT testing continued for eight trials starting from the trial prior to the first negative response. The algorithm imple mented in this study used false positive detection tests in which no vibrotactile stimulus was presented, but the participant was expected to respond. These false positive trials were implemented in 20% of the successive trials, and on detection of a false positive trial, it was discarded and a new trial was restarted. The number of trials (n = 8) included in threshold estimation was chosen in order to attain an accuracy of ±2 dB and this number excludes the false positive trials. As per the S1UD algorithm, a required accuracy of ±1 dB would entail the use of 26 non-false positive trials. In this study, we estimated the VDTs for six different frequencies in three different stimulation sites (n = 18), and in order to reduce the strain on the subjects we concluded that an accuracy of ±2 dB is adequate. S t a t is t ic a l a n a ly s is
A repeated measures ANOVA was performed using Minitab’' statistics software (version 16). A mixed-model was utilized to assess the dependence of VDTs on age and sex (between subjects), and stimulation frequency and site (within subjects).
Results
The statistical analysis revealed VDTs were significantly dependent on stimulus site (F = 132.99, p < 0.0001), fre quency of stimulation (F = 128.98,/?
