- Email: [email protected]
Anisotropy and spatial tactile acuity on human lips
Clinical Neurophysiology 123 (2012) 1593–1598
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Anisotropy and spatial tactile acuity on human lips Gabrielle Todd ⇑ Discipline of Physiology, University of Adelaide, Adelaide, Australia School of Pharmacy and Medical Sciences, Sansom Institute, University of South Australia, Adelaide, Australia
a r t i c l e
i n f o
Article history: Accepted 17 January 2012 Available online 14 February 2012 Keywords: Anisotropy Spatial tactile acuity Gratings orientation Human Lip
h i g h l i g h t s Spatial tactile acuity is greater on the upper lip than on the lower lip in humans. A property of spatial tactile acuity known as anisotropy (or directional dependence) is absent on human lips. The lack of anisotropy on human lips is surprising given that anisotropy is present on the finger and that mechanoreceptor afferents that supply human lips exhibit similar characteristics to those of the hand.
a b s t r a c t Objective: To investigate tactile anisotropy on human lips. Methods: Spatial tactile acuity was assessed with a three-alternative, forced-choice grating orientation task. Circular probes with horizontal (parallel to lip), vertical (perpendicular to lip), or oblique (45° right of vertical) grooves and ridges of equal width were applied (n = 60) to the midline of each lip. Participants (n = 13) were asked to state the grating orientation whilst blindfolded. The percentage of correct responses was plotted as a function of the log gap width. Data were fitted with a four-parameter sigmoid function. Response bias was assessed (n = 13) with application of a smooth polished Perspex probe. 65.5%, 71.5%, and 63.0% correct was adopted as the threshold estimate for the vertical, horizontal, and oblique orientations based on the measured response bias. Results: Across orientations, the threshold on the upper lip (1.5 ± 0.9 mm) was significantly greater than on the lower lip (1.0 ± 0.7 mm; P = 0.006). However, there was no significant main effect of orientation or orientation-by-lip interaction on threshold. Conclusion: Tactile anisotropy is absent on human lips. Significance: The lack of anisotropy is surprising given that anisotropy is present on fingers and that afferent input and sensory processing for human lips and fingers share similarities. Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In humans and primates, the lips, tongue, and fingers are welladapted to processing spatial information due to their dense receptor innervation (Johansson and Vallbo, 1979; Darian-Smith and Kenins, 1980; Halata and Munger, 1983) and large areas of representation in the somatosensory cortex (Dreyer et al., 1975; Nelson et al., 1980). Human spatial tactile acuity has been studied with the use of psychophysical methods such as two-point discrimination and the grating orientation task (two-alternative, forcedchoice tasks). The latter involves gently pressing hemispherical plastic probes on the skin. Each probe has grooves and ridges of ⇑ Address: School of Pharmacy and Medical Sciences, University of South Australia, GPO Box 2471, Adelaide SA 5001, Australia. Tel.: +61 8 8302 1979; fax: +61 8 8302 2389. E-mail address: [email protected]
equal width (0.25–3.5 mm). Human and primate experiments have shown that this stimulus primarily activates slowly-adapting afferent fibres (Johnson and Phillips, 1981; Phillips and Johnson, 1981). The probe is usually applied with the grooves in one of two orientations (0° and 90°). Blindfolded participants are asked to discriminate the orientation of the grating. Gratings of successively narrower widths are used to determine the threshold for spatial tactile acuity (Johnson and Phillips, 1981). The threshold for spatial tactile acuity of the glabrous skin of the lips (0.51–1.06 mm) has been found to be lower than on the finger pad of the index finger (0.94–1.26 mm) (Van Boven and Johnson, 1994a; Sathian and Zangaladze, 1996; Patel et al., 1997; Vega-Bermudez and Johnson, 2001, 2004; Grant et al., 2006). The current study used a modified grating orientation task to investigate a property of spatial tactile acuity known as anisotropy (or directional dependence). The modified task involves a threealternative, forced-choice grating orientation protocol (Gibson
1388-2457/$36.00 Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2012.01.007
1594
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
and Craig, 2005). Three orientations are used (instead of two) so that subjects are forced to rely on spatial cues rather than intensive cues to determine the orientation of the grating. This method has revealed anisotropy on the human finger pad and at the base of the index finger (between the proximal interphalangeal and metacarophalangeal joints). At both locations, acuity is greatest in the proximal–distal orientation (along the axis of the finger) (Gibson and Craig, 2005). Anisotropy has also been observed in other areas of the body, on glabrous and non-glabrous skin, using two-alternative, forced-choice measures of spatial tactile acuity (e.g. gap detection task, two-point discrimination, and grating orientation task) in humans (Wong et al., 1974; Green, 1982; Fuchs and Brown, 1984; Lechelt, 1988; Essock et al., 1992, 1997; Stevens and Patterson, 1995; Wheat and Goodwin, 2000; Vega-Bermudez and Johnson, 2004; Gibson and Craig, 2005; c.f. Craig, 1999) and primates (Phillips and Johnson, 1981; Wheat and Goodwin, 2000). Anisotropy is thought to be due to greater skin compliance when probes are applied parallel to the skin ridges (VegaBermudez and Johnson, 2004). The size and shape of receptive fields (Stevens and Patterson, 1995) and orientation-selective neurones in somatosensory cortex (Essock et al., 1992, 1997) have also been proposed as potential mechanisms for tactile anisotropy. The aim of the present study was to investigate anisotropy on the glabrous skin of human lips. It was hypothesised that spatial tactile acuity would be (a) similar on the upper and lower lip and (b) anisotropy would be present on the upper and lower lip with greater acuity in a horizontal orientation (parallel to the lip) than in a vertical orientation (perpendicular to the lip). The midline of the lip was investigated due to overlap of sensory afferents across this region (Fuchs and Brown, 1984; Hwang et al., 2004). Investigation of anisotropy and spatial tactile acuity on human lips is important for monitoring or treating speech disorders and trigeminal sensory dysfunction that accompany stroke and other neurological disorders.
probe kit consisted of a set of 10 hemispherical plastic probes (19 mm in diameter) with grooves and ridges of equal width. Each probe has a different grid spacing (0.25–3.50 mm) and the depth of the grooves prevents the skin from touching the base of each groove (Fig. 1). The reliability and validity of the Tactile Acuity Grids probe kit for the assessment of spatial tactile acuity has been established previously (Van Boven and Johnson, 1994a). The author applied the probes to all subjects. The author undertook training to apply the probe for 1–2 s at a constant force (1–1.5 N). Force application was checked between experiments with the use of a strain gauge (Load Cell model MLP-1000; Transducer Techniques, Temecula CA, USA). 2.2. Protocol 2.2.1. Experiment one A three-alternative, forced-choice grating orientation protocol was used (Gibson and Craig, 2005). Subjects (n = 13, 4 male and 9 female, age 23 ± 3 years), were instructed to sit comfortably and partly open their mouth (1–2 cm). The midline of the upper and lower lip was determined by measurement of the midpoint between the right and left labial commissure and marked. Subjects were then blind-folded. Each lip was tested separately and in pseudorandom order. For each lip, one probe was randomly selected and applied 60 times, 20 times with the grooves in a horizontal orientation (parallel to the lip), 20 times with the grooves vertical (perpendicular to the lip), and 20 times with the grooves oblique (45° to the right of vertical). Subjects were informed of the total number of applications but not the number of applications per orientation. The order of presentation in the horizontal, vertical, and oblique orientations was pseudorandom. After each application, the subject informed the experimenter whether they perceived the grooves to be horizontal, vertical, or oblique. No feedback of correct or incorrect responses was given. The procedure was repeated for the remaining nine probe widths.
2. Methods Twenty-three healthy adults (10 male, 13 female, age 29 ± 9 years) participated in the study. Thirteen subjects participated in experiment one and 13 subjects participated in experiment two (i.e. 3 subjects participated in both experiments). All were free of neurological symptoms and facial scarring. The experimental procedures were approved by The University of Adelaide Human Research Ethics Committee and were conducted according to the Declaration of Helsinki. Written informed consent was obtained. 2.1. Spatial tactile acuity Spatial tactile acuity was assessed with a Tactile Acuity Grids probe kit (TAG JVC Domes Kit, MedCore, St. Louis, MO, USA). The
A
B Cross section
2.2.2. Experiment two Response bias within the three-alternative, forced-choice grating orientation protocol was assessed with application of a smooth polished Perspex probe manufactured to be similar in size and contour to probes in the Tactile Acuity Grids probe kit. Subjects (n = 13, 8 male and 5 female, age 33 ± 10 years) were told that a probe from the Tactile Acuity Grids probe kit was going to be applied 30 times to their lip with the grooves in a horizontal (parallel to the lip), vertical (perpendicular to the lip), or oblique (45° to the right of vertical) orientation. Subjects were asked to report if they perceived the grooves to be horizontal, vertical, or oblique in orientation after each application. Subjects were informed of the total number of applications but not the number of applications per orientation. Subjects were instructed to sit comfortably, partly open
Top view Vertical
Horizontal
Oblique
1 cm 1 cm Fig. 1. Experimental apparatus. Spatial tactile acuity was assessed with a Tactile Acuity Grids probe kit (TAG JVC Domes Kit, MedCore, St. Louis, MO, USA). The probe kit consisted of a set of 10 hemispherical plastic probes (19 mm in diameter) with grooves and ridges of equal width (0.25–3.50 mm). (A) Cross section of one probe. Each probe was applied to the lip in three orientations (horizontal, vertical, and oblique). (B) Top view of each orientation.
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
their mouth (1–2 cm), and were then blind-folded. The probe from the Tactile Acuity Grids probe kit that was used to instruct the subject was then substituted with the smooth polished probe. The smooth polished probe was applied 30 times to the midpoint of the lower lip. No feedback was provided to the subject. 2.3. Data analysis Threshold was determined with the method described by Gibson and Craig (2005). The percentage of correct responses was plotted as a function of the log of the gap width (e.g. Fig. 2). The data were fitted with a four-parameter sigmoid function (Eq. (1)) with two constrained parameters (y0 and a).
y ¼ y0 þ
a 1 þ eð
xx0 b
ð1Þ
Þ
Unlike previous studies performed on the finger tip (Van Boven and Johnson, 1994b; Vega-Bermudez and Johnson, 2004; Gibson and Craig, 2005), the value of the constraints was set separately for each orientation based on the response bias quantified in experiment two. For the vertical orientation, y0 = 31 and a = 65.5 (i.e. function fit between 31% and 100% correct performance). For the horizontal orientation, y0 = 43 and a = 71.5 (i.e. function fit between 43% and 100% correct performance). For the oblique orientation, y0 = 26 and a = 63 (i.e. function fit between 26% and 100% correct performance). 65.5%, 71.5%, and 63.0% correct was adopted as the threshold estimate for the vertical, horizontal, and oblique orientations, respectively. To determine threshold, Eq. (1) was used to calculate x for a known value of y (vertical: 65.5% correct; horizontal: 71.5% correct; oblique: 63.0% correct). The overall threshold for each lip was calculated with the constraints set at y0 = 33.33 and a = 66.66 (i.e. function fit between 33.33% and 66.66% correct performance). For data that did not converge into a four-parameter sigmoid function, threshold was determined by interpolation between groove widths that corresponded to just above and below the criterion (vertical: 65.5% correct; horizontal: 71.5% correct; oblique: 63.0% correct). Group data are presented in the text as mean ± standard deviation (SD) and in figures as mean ± standard error of the mean. Group response bias (experiment two) was analysed with one-way
1595
repeated measures analysis of variance (RM ANOVA) for comparison of response (%) in each orientation (vertical, horizontal, oblique). Group threshold data (experiment one) was analysed with two-way repeated measures ANOVA for comparison between lips (upper and lower) and grating orientation (horizontal, vertical, and oblique) (Sigmastat, 3.11, Systat Software Inc, Point Richmond, USA). A paired t-test was used for comparison of the overall threshold on the upper and lower lip. Statistical significance was set at 5%. 3. Results 3.1. Response bias Response bias within the three-alternative, forced-choice grating orientation protocol was assessed with application of a smooth polished Perspex probe whilst the volunteer was blindfolded (experiment two). On average, volunteers answered vertical in 31 ± 12% of trials, horizontal in 43 ± 15% of trials, and oblique in 26 ± 10% of trials. The percent response differed significantly between orientations (P = 0.03). Volunteers answered horizontal significantly more than oblique (P = 0.026) and volunteers tended to answer horizontal more than vertical (P = 0.07). Thus, the threshold criterion was set at 65.5% for the vertical orientation, 71.5% for the horizontal orientation, and 63.0% for the oblique orientation. 3.2. Threshold The average r2 for determination of threshold on the upper and lower lip was 0.85 ± 0.08 and 0.87 ± 0.05, respectively. The average r2 for determination of threshold in the vertical, horizontal, and oblique orientations was 0.72 ± 0.19, 0.62 ± 0.10, and 0.76 ± 0.09, respectively. There were seven instances (of a possible 78) where one of the orientations did not converge into a four-parameter sigmoid function. In these cases, threshold was determined by interpolation between the groove widths that corresponded to just above and below the threshold criterion for that orientation. The average overall threshold on the upper lip (1.5 ± 0.9 mm) was significantly greater than on the lower lip (1.0 ± 0.7 mm; paired t-test, P = 0.006). There was no significant main effect of orientation or lip on threshold and there was no significant orientation-by-lip interaction (Fig. 3).
100
Correct responses (%)
4. Discussion 80
The aim of the current study was to investigate anisotropy on the glabrous skin of human lips. The results demonstrate that spatial tactile acuity is greater on the lower lip than on the upper lip and anisotropy is absent at the midline.
H V O
60
4.1. Spatial tactile acuity
40
20
Horizontal Vertical Oblique
0 0.1
1
10
Grating width (mm) Fig. 2. Single subject data from experiment one showing the percentage of correct responses for each orientation as a function of the log grating width (mm). Data for the horizontal (circle), vertical (triangle), and oblique (square) orientations are fitted with a four-parameter sigmoid function (see Section 2). Long dash, horizontal function. Short dash, vertical function. Dotted line, oblique function. The group threshold estimate was 65.5%, 71.5%, and 63.0% for the vertical (V), horizontal (H), and oblique (O) orientations, respectively (based on the response bias measured in experiment two). The group threshold estimate for each orientation is marked on the y-axis.
Spatial tactile acuity and anisotropy was investigated at the midline of the upper and lower lip due to bilateral overlap of peripheral nerves in this region. Overlap of peripheral nerves at the midline is likely to increase the density of mechanoreceptive afferents and thus the total number of neurons responding to a particular stimulus. Enhanced acuity at midline structures has been reported for the lips, oral mucosa, tongue, and skin on the back when tested with two-point discrimination (Ringel and Ewanowski, 1965; Lass et al., 1972; Fuchs and Brown, 1984; Rath and Essick, 1990). At the midline, the average threshold on the lower lip (1.0 ± 0.7 mm) was significantly less than on the upper lip (1.5 ± 0.9 mm). This suggests that spatial tactile acuity was greater on the lower lip than on the upper lip. Enhanced spatial tactile acu-
A
B
100
80 H V O
60
40
Horizontal Vertical Oblique
20
0 0.1
1
10
Average lower lip correct responses (%)
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
Average upper lip correct responses (%)
1596
100
80
60
40
0 0.1
0.8
0.4
0
10
1.6
Average lower lip threshold (mm)
Average upper lip threshold (mm)
1.2
1
Grating width (mm)
D
1.6
Horizontal Vertical Oblique
20
Grating width (mm)
C
H V O
1.2
0.8
0.4
0 Vertical
Horizontal
Oblique
Orientation
Vertical
Horizontal
Oblique
Orientation
Fig. 3. Group data for experiment one showing the percentage of correct responses and threshold for each orientation on the upper and lower lip. Percentage of correct responses for each orientation is shown as a function of the log grating width (mm) for the upper lip (A) and lower lip (B). Data for the horizontal (circle), vertical (triangle), and oblique (square) orientations are fitted with a four-parameter sigmoid function (see Section 2). Long dash, horizontal function. Short dash, vertical function. Dotted line, oblique function. The threshold estimate was 65.5%, 71.5%, and 63.0% for the vertical, horizontal, and oblique orientations, respectively (based on the response bias measured in experiment two). The threshold estimate for each orientation is marked on the y-axis. The average threshold for each orientation is shown for the upper lip (C) and lower lip (D).
ity has also been observed on the lower lip (non-midline) with a two-choice grating orientation task (Patel et al., 1997; c.f. Wohlert, 1996). The difference in spatial tactile acuity between lips is most likely due to differences in innervation. The upper lip is innervated by the infraorbital nerve whereas the lower lip is innervated by the mental nerve. Regional differences in the type and density of mechanoreceptors or differences in the processing of afferent signals from the lips in the somatosensory cortex could also contribute. However, regional differences in the type and density of receptors on the lips has not been investigated and variation in the representation of lip regions on the somatosensory cortex is unlikely based on microelectrode recordings in Macaques (Nelson et al., 1980). 4.2. Anisotropy Investigation of anisotropy requires careful consideration of response bias. Gibson and Craig (2005) assessed response bias by calculating the ‘hit and false alarm’ rates for each orientation in a three-choice grating orientation task on the finger pad. The proportion of correct responses was then corrected for response bias for each orientation separately prior to determination of threshold. Using this approach, the authors confirmed the presence of anisotropy on the finger pad and at the base of the finger (Gibson and Craig, 2005). The presence of anisotropy on the finger confirmed the findings of an earlier study that used a two-choice grating orien-
tation task that assumed equal response bias between orientations and inferred equal response bias by comparing the percentage of correct responses for the two orientations at the smallest grating width (0.35 mm) (Vega-Bermudez and Johnson, 2004). In the current study, response bias was quantified in a largely independent group with the use of a smooth polished probe. Subjects were shown a probe with gratings and told that the gratings would be applied to the lip in three orientations. Subjects were then blindfolded and the smooth polished probe was applied to the lip instead of the probe with gratings. The results of the current study indicate that response bias is not equal between orientations. Volunteers answered horizontal (43 ± 15% of trials) significantly more than oblique (26 ± 10% of trials) and volunteers tended to answer horizontal more than vertical (31 ± 12% of trials). Thus, in the current study threshold was set separately for each orientation. When response bias was taken into account, there was no significant difference in threshold for the horizontal, vertical, and oblique orientations. This suggests that anisotropy is absent at the midline on human lips. Earlier reports of anisotropy on the lips are likely due to use of a two-choice grating orientation task, lack of measurement of response bias (Wohlert, 1996), or assumed equal response bias between orientations (Patel et al., 1997). The lack of anisotropy on the lips is surprising given that anisotropy is present on the finger and the finger and lips share similarities in sensation. On the finger pad and at the base of the index finger, acuity is greatest in the proximal–distal orientation (along
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
the axis of the finger) (Essock et al., 1992; Gibson and Craig, 2005). This orientation is parallel to the skin ridges and has the greatest skin compliance. The size and shape of receptive fields (Stevens and Patterson, 1995) and orientation-selective neurones in somatosensory cortex (Essock et al., 1992, 1997) have also been proposed as potential mechanisms for tactile anisotropy in the finger. Measurements of skin compliance and skin ridge orientation on human lips are not available. However, mechanoreceptor afferents that supply human lips exhibit similar characteristics to those of the hand. There are slowly adapting (SA) afferents on lips that resemble SA I afferents in hairy and glabrous skin of the hand. These afferents exhibit a high dynamic sensitivity and an irregular discharge during tissue deformation. There are also SA afferents on lips that resemble SA II afferents in the hand. These afferents exhibit spontaneous activity, a regular discharge rate, and a high sensitivity to lateral skin stretch (for review see Trulsson and Johansson, 2002). It is also worth noting that anisotropy is not limited to the somatosensory system. Anisotropy is also present in the human visual system. Visual acuity is greater when lines and edges are orientated horizontally or vertically as opposed to obliquely. Visual anisotropy is thought to be due to a greater proportion of cells that are selectively tuned to horizontal and vertical orientations rather than oblique orientations (for review see Appelle, 1972). The use of a grating orientation task to assess anisotropy and spatial tactile acuity on the lips is superior to that of two-point discrimination and gap detection for several reasons. First, the overall dimensions, edge contact, and contact area of the probe is similar regardless of the grating orientation thus eliminating non-spatial cues. Second, the threshold for a grating orientation task at the finger tip corresponds to the mean center-to-center spacing between slowly adapting afferent fibres in primate (macaque; 1.3 mm) and human skin (1.4 mm) (Johansson and Vallbo, 1979; DarianSmith and Kenins, 1980). Third, threshold measured with the grating orientation task is consistent with that obtained with more complex stimuli such as letters and Braille characters. Lastly, the underlying mechanisms for acuity in the grating orientation task are better understood than for two-point discrimination. Even so, there is a possible limitation to the use of the grating orientation task on the lips. The surface area of the upper and lower lip differs as does the surface area at the midline and the side of the lip. Thus, the proportion of glabrous and non-glabrous skin activated by the probe may differ between lip positions. Glabrous skin has greater acuity for two-point discrimination than non-glabrous skin (on the upper lip) possibly due to an increased density of mechanoreceptive afferents and smaller receptive field size for slowly adapting afferent fibres (Chen et al., 1995). The use of smaller grating probes may resolve this issue in future studies. Other points to consider when using a grating orientation task are that threshold increases with age, women tend to have a lower threshold than men (Wohlert, 1996; c.f. Patel et al., 1997), and threshold can improve by 2% between sessions (Van Boven and Johnson, 1994a). In summary, the results of the current study demonstrate that spatial tactile acuity is greater on the lower lip than on the upper lip and that anisotropy is absent on human lips. The greater spatial tactile acuity on the lower lip has implications for speech pathologists and clinicians. Although speech can be accomplished with limited auditory or tactile input (e.g. Kelso and Tuller, 1983), afferent input is required for adaptation to lip perturbation (Abbs and Gracco, 1984) and the formation of speech motor programs (e.g. Gracco and Abbs, 1985). This fits with the common experience that speech is often slurred when the lips are anaesthetised during dental treatment. The results of the current study suggest that sensation on the lower lip may be more important for speech than sensation on the upper lip. Tests of spatial tactile acuity have also been used to monitor recovery of sensation in patients with nerve damage resulting from trauma or elective jaw surgery
1597
(Van Boven and Johnson, 1994b). The results of the current study suggest that monitoring spatial tactile acuity over time requires determination of response bias and application of a constant set of orientations. Acknowledgements The author holds an Australian National Health and Medical Research Council Career Development Award. The author wishes to thank Ms. Heather J. Jarred, Mr. Peter D.F. Varacalli, Ms. Stefanie Heigele, and Mr. Benjamin D. Noll for assisting with collection of pilot data and Prof. Timothy S. Miles for advice during manuscript preparation. References Abbs JH, Gracco VL. Control of complex motor gestures: orofacial muscle responses to load perturbations of lip during speech. J Neurophysiol 1984;51:705–23. Appelle S. Perception and discrimination as a function of stimulus orientation: the ‘‘oblique effect’’ in man and animals. Psychol Bull 1972;78:266–78. Chen CC, Essick GK, Kelly DG, Young MG, Nestor JM, Masse B. Gender-, side- and site-dependent variations in human perioral spatial resolution. Arch Oral Biol 1995;40:539–48. Craig JC. Grating orientation as a measure of tactile spatial acuity. Somatosens Mot Res 1999;16:197–206. Darian-Smith I, Kenins P. Innervation density of mechanoreceptive fibres supplying glabrous skin of the monkey’s index finger. J Physiol 1980;309:147–55. Dreyer DA, Loe PR, Metz CB, Whitsel BL. Representation of head and face in postcentral gyrus of the macaque. J Neurophysiol 1975;38:714–33. Essock EA, Krebs WK, Prather JR. An anisotropy of human tactile sensitivity and its relation to the visual oblique effect. Exp Brain Res 1992;91:520–4. Essock EA, Krebs WK, Prather JR. Superior sensitivity for tactile stimuli orientated proximally-distally on the finger: implications for mixed Class 1 and Class 2 anisotropies. J Exp Psychol Hum Percept Perform 1997;23:515–27. Fuchs JL, Brown PB. Two-point discriminability: relation to properties of the somatosensory system. Somatosens Res 1984;2:163–9. Gibson GO, Craig JC. Tactile spatial sensitivity and anisotropy. Percept Psychophys 2005;67:1061–79. Gracco VL, Abbs JH. Dynamic control of the perioral system during speech: kinematic analyses of autogenic and nonautogenic sensorimotor processes. J Neurophysiol 1985;54:418–32. Grant AC, Fernandez R, Shilian P, Yanni E, Hill MA. Tactile spatial acuity differs between fingers: a study comparing two testing paradigms. Percept Psychophys 2006;68:1359–62. Green BG. The perception of distance and location for dual tactile pressures. Percept Psychophys 1982;31:315–23. Halata Z, Munger BL. The sensory innervation of primate facial skin. II. Vermilion border and mucosa of lip. Brain Res 1983;286:81–107. Hwang K, Suh MS, Chung IH. Cutaneous distribution of infraorbital nerve. J Craniofac Surg 2004;15:3–5. Johansson RS, Vallbo AB. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 1979;286:283–300. Johnson KO, Phillips JR. Tactile spatial resolution. I. Two-point discrimination, gap detection, grating resolution, and letter recognition. J Neurophysiol 1981;46:1177–92. Kelso JA, Tuller B. ‘‘Compensatory articulation’’ under conditions of reduced afferent information: a dynamic formulation. J Speech Hear Res 1983;26:217–24. Lass NJ, Kotchek CL, Deem JF. Oral two-point discrimination: further evidence of asymmetry on right and left sides of selected oral structures. Percept Mot Skills 1972;35:59–67. Lechelt EC. Spatial asymmetries in tactile discrimination of line orientation: a comparison of the sighted, visually impaired, and blind. Perception 1988;17:579–85. Nelson RJ, Sur M, Felleman DJ, Kaas JH. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J Comp Neurol 1980;192:611–43. Patel J, Essick GK, Kelly DG. Utility of square-wave gratings to assess perioral spatial acuity. J Oral Maxillofac Surg 1997;55:593–601. Phillips JR, Johnson KO. Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. J Neurophysiol 1981;46:1192–203. Rath EM, Essick GK. Perioral somesthetic sensibility: do the skin of the lower face and the midface exhibit comparable sensitivity? J Oral Maxillofac Surg 1990;48:1181–90. Ringel RL, Ewanowski SJ. Oral perception. I. Two-point discrimination. J Speech Hear Res 1965;8:389–98. Sathian K, Zangaladze A. Tactile spatial acuity at the human fingertip and lip: bilateral symmetry and interdigit variability. Neurology 1996;46:1464–6. Stevens JC, Patterson MQ. Dimensions of spatial acuity in the touch sense: changes over the life span. Somatosens Mot Res 1995;12:29–47.
1598
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
Trulsson M, Johansson RS. Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors. Behav Brain Res 2002;135:27–33. Van Boven RW, Johnson KO. The limit of tactile spatial resolution in humans: grating orientation discrimination at the lip, tongue, and finger. Neurology 1994a;44:2361–6. Van Boven RW, Johnson KO. A psychophysical study of the mechanisms of sensory recovery following nerve injury in humans. Brain 1994b;117:149–67. Vega-Bermudez F, Johnson KO. Differences in spatial acuity between digits. Neurology 2001;56:1389–91.
Vega-Bermudez F, Johnson KO. Fingertip skin conformance accounts, in part, for differences in tactile spatial acuity in young subjects, but not for the decline in spatial acuity with aging. Percept Psychophys 2004;66:60–7. Wheat HE, Goodwin AW. Tactile discrimination of gaps by slowly adapting afferents: effects of population parameters and anisotropy in the fingerpad. J Neurophysiol 2000;84:1430–44. Wohlert AB. Tactile perception of spatial stimuli on the lip surface by young and older adults. J Speech Hear Res 1996;39:1191–8. Wong TS, Ho R, Ho J. Influence of shape of receptor organ on the horizontal–vertical illusion in passive touch. J Exp Psychol 1974;103:414–9.
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Anisotropy and spatial tactile acuity on human lips Gabrielle Todd ⇑ Discipline of Physiology, University of Adelaide, Adelaide, Australia School of Pharmacy and Medical Sciences, Sansom Institute, University of South Australia, Adelaide, Australia
a r t i c l e
i n f o
Article history: Accepted 17 January 2012 Available online 14 February 2012 Keywords: Anisotropy Spatial tactile acuity Gratings orientation Human Lip
h i g h l i g h t s Spatial tactile acuity is greater on the upper lip than on the lower lip in humans. A property of spatial tactile acuity known as anisotropy (or directional dependence) is absent on human lips. The lack of anisotropy on human lips is surprising given that anisotropy is present on the finger and that mechanoreceptor afferents that supply human lips exhibit similar characteristics to those of the hand.
a b s t r a c t Objective: To investigate tactile anisotropy on human lips. Methods: Spatial tactile acuity was assessed with a three-alternative, forced-choice grating orientation task. Circular probes with horizontal (parallel to lip), vertical (perpendicular to lip), or oblique (45° right of vertical) grooves and ridges of equal width were applied (n = 60) to the midline of each lip. Participants (n = 13) were asked to state the grating orientation whilst blindfolded. The percentage of correct responses was plotted as a function of the log gap width. Data were fitted with a four-parameter sigmoid function. Response bias was assessed (n = 13) with application of a smooth polished Perspex probe. 65.5%, 71.5%, and 63.0% correct was adopted as the threshold estimate for the vertical, horizontal, and oblique orientations based on the measured response bias. Results: Across orientations, the threshold on the upper lip (1.5 ± 0.9 mm) was significantly greater than on the lower lip (1.0 ± 0.7 mm; P = 0.006). However, there was no significant main effect of orientation or orientation-by-lip interaction on threshold. Conclusion: Tactile anisotropy is absent on human lips. Significance: The lack of anisotropy is surprising given that anisotropy is present on fingers and that afferent input and sensory processing for human lips and fingers share similarities. Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In humans and primates, the lips, tongue, and fingers are welladapted to processing spatial information due to their dense receptor innervation (Johansson and Vallbo, 1979; Darian-Smith and Kenins, 1980; Halata and Munger, 1983) and large areas of representation in the somatosensory cortex (Dreyer et al., 1975; Nelson et al., 1980). Human spatial tactile acuity has been studied with the use of psychophysical methods such as two-point discrimination and the grating orientation task (two-alternative, forcedchoice tasks). The latter involves gently pressing hemispherical plastic probes on the skin. Each probe has grooves and ridges of ⇑ Address: School of Pharmacy and Medical Sciences, University of South Australia, GPO Box 2471, Adelaide SA 5001, Australia. Tel.: +61 8 8302 1979; fax: +61 8 8302 2389. E-mail address: [email protected]
equal width (0.25–3.5 mm). Human and primate experiments have shown that this stimulus primarily activates slowly-adapting afferent fibres (Johnson and Phillips, 1981; Phillips and Johnson, 1981). The probe is usually applied with the grooves in one of two orientations (0° and 90°). Blindfolded participants are asked to discriminate the orientation of the grating. Gratings of successively narrower widths are used to determine the threshold for spatial tactile acuity (Johnson and Phillips, 1981). The threshold for spatial tactile acuity of the glabrous skin of the lips (0.51–1.06 mm) has been found to be lower than on the finger pad of the index finger (0.94–1.26 mm) (Van Boven and Johnson, 1994a; Sathian and Zangaladze, 1996; Patel et al., 1997; Vega-Bermudez and Johnson, 2001, 2004; Grant et al., 2006). The current study used a modified grating orientation task to investigate a property of spatial tactile acuity known as anisotropy (or directional dependence). The modified task involves a threealternative, forced-choice grating orientation protocol (Gibson
1388-2457/$36.00 Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2012.01.007
1594
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
and Craig, 2005). Three orientations are used (instead of two) so that subjects are forced to rely on spatial cues rather than intensive cues to determine the orientation of the grating. This method has revealed anisotropy on the human finger pad and at the base of the index finger (between the proximal interphalangeal and metacarophalangeal joints). At both locations, acuity is greatest in the proximal–distal orientation (along the axis of the finger) (Gibson and Craig, 2005). Anisotropy has also been observed in other areas of the body, on glabrous and non-glabrous skin, using two-alternative, forced-choice measures of spatial tactile acuity (e.g. gap detection task, two-point discrimination, and grating orientation task) in humans (Wong et al., 1974; Green, 1982; Fuchs and Brown, 1984; Lechelt, 1988; Essock et al., 1992, 1997; Stevens and Patterson, 1995; Wheat and Goodwin, 2000; Vega-Bermudez and Johnson, 2004; Gibson and Craig, 2005; c.f. Craig, 1999) and primates (Phillips and Johnson, 1981; Wheat and Goodwin, 2000). Anisotropy is thought to be due to greater skin compliance when probes are applied parallel to the skin ridges (VegaBermudez and Johnson, 2004). The size and shape of receptive fields (Stevens and Patterson, 1995) and orientation-selective neurones in somatosensory cortex (Essock et al., 1992, 1997) have also been proposed as potential mechanisms for tactile anisotropy. The aim of the present study was to investigate anisotropy on the glabrous skin of human lips. It was hypothesised that spatial tactile acuity would be (a) similar on the upper and lower lip and (b) anisotropy would be present on the upper and lower lip with greater acuity in a horizontal orientation (parallel to the lip) than in a vertical orientation (perpendicular to the lip). The midline of the lip was investigated due to overlap of sensory afferents across this region (Fuchs and Brown, 1984; Hwang et al., 2004). Investigation of anisotropy and spatial tactile acuity on human lips is important for monitoring or treating speech disorders and trigeminal sensory dysfunction that accompany stroke and other neurological disorders.
probe kit consisted of a set of 10 hemispherical plastic probes (19 mm in diameter) with grooves and ridges of equal width. Each probe has a different grid spacing (0.25–3.50 mm) and the depth of the grooves prevents the skin from touching the base of each groove (Fig. 1). The reliability and validity of the Tactile Acuity Grids probe kit for the assessment of spatial tactile acuity has been established previously (Van Boven and Johnson, 1994a). The author applied the probes to all subjects. The author undertook training to apply the probe for 1–2 s at a constant force (1–1.5 N). Force application was checked between experiments with the use of a strain gauge (Load Cell model MLP-1000; Transducer Techniques, Temecula CA, USA). 2.2. Protocol 2.2.1. Experiment one A three-alternative, forced-choice grating orientation protocol was used (Gibson and Craig, 2005). Subjects (n = 13, 4 male and 9 female, age 23 ± 3 years), were instructed to sit comfortably and partly open their mouth (1–2 cm). The midline of the upper and lower lip was determined by measurement of the midpoint between the right and left labial commissure and marked. Subjects were then blind-folded. Each lip was tested separately and in pseudorandom order. For each lip, one probe was randomly selected and applied 60 times, 20 times with the grooves in a horizontal orientation (parallel to the lip), 20 times with the grooves vertical (perpendicular to the lip), and 20 times with the grooves oblique (45° to the right of vertical). Subjects were informed of the total number of applications but not the number of applications per orientation. The order of presentation in the horizontal, vertical, and oblique orientations was pseudorandom. After each application, the subject informed the experimenter whether they perceived the grooves to be horizontal, vertical, or oblique. No feedback of correct or incorrect responses was given. The procedure was repeated for the remaining nine probe widths.
2. Methods Twenty-three healthy adults (10 male, 13 female, age 29 ± 9 years) participated in the study. Thirteen subjects participated in experiment one and 13 subjects participated in experiment two (i.e. 3 subjects participated in both experiments). All were free of neurological symptoms and facial scarring. The experimental procedures were approved by The University of Adelaide Human Research Ethics Committee and were conducted according to the Declaration of Helsinki. Written informed consent was obtained. 2.1. Spatial tactile acuity Spatial tactile acuity was assessed with a Tactile Acuity Grids probe kit (TAG JVC Domes Kit, MedCore, St. Louis, MO, USA). The
A
B Cross section
2.2.2. Experiment two Response bias within the three-alternative, forced-choice grating orientation protocol was assessed with application of a smooth polished Perspex probe manufactured to be similar in size and contour to probes in the Tactile Acuity Grids probe kit. Subjects (n = 13, 8 male and 5 female, age 33 ± 10 years) were told that a probe from the Tactile Acuity Grids probe kit was going to be applied 30 times to their lip with the grooves in a horizontal (parallel to the lip), vertical (perpendicular to the lip), or oblique (45° to the right of vertical) orientation. Subjects were asked to report if they perceived the grooves to be horizontal, vertical, or oblique in orientation after each application. Subjects were informed of the total number of applications but not the number of applications per orientation. Subjects were instructed to sit comfortably, partly open
Top view Vertical
Horizontal
Oblique
1 cm 1 cm Fig. 1. Experimental apparatus. Spatial tactile acuity was assessed with a Tactile Acuity Grids probe kit (TAG JVC Domes Kit, MedCore, St. Louis, MO, USA). The probe kit consisted of a set of 10 hemispherical plastic probes (19 mm in diameter) with grooves and ridges of equal width (0.25–3.50 mm). (A) Cross section of one probe. Each probe was applied to the lip in three orientations (horizontal, vertical, and oblique). (B) Top view of each orientation.
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
their mouth (1–2 cm), and were then blind-folded. The probe from the Tactile Acuity Grids probe kit that was used to instruct the subject was then substituted with the smooth polished probe. The smooth polished probe was applied 30 times to the midpoint of the lower lip. No feedback was provided to the subject. 2.3. Data analysis Threshold was determined with the method described by Gibson and Craig (2005). The percentage of correct responses was plotted as a function of the log of the gap width (e.g. Fig. 2). The data were fitted with a four-parameter sigmoid function (Eq. (1)) with two constrained parameters (y0 and a).
y ¼ y0 þ
a 1 þ eð
xx0 b
ð1Þ
Þ
Unlike previous studies performed on the finger tip (Van Boven and Johnson, 1994b; Vega-Bermudez and Johnson, 2004; Gibson and Craig, 2005), the value of the constraints was set separately for each orientation based on the response bias quantified in experiment two. For the vertical orientation, y0 = 31 and a = 65.5 (i.e. function fit between 31% and 100% correct performance). For the horizontal orientation, y0 = 43 and a = 71.5 (i.e. function fit between 43% and 100% correct performance). For the oblique orientation, y0 = 26 and a = 63 (i.e. function fit between 26% and 100% correct performance). 65.5%, 71.5%, and 63.0% correct was adopted as the threshold estimate for the vertical, horizontal, and oblique orientations, respectively. To determine threshold, Eq. (1) was used to calculate x for a known value of y (vertical: 65.5% correct; horizontal: 71.5% correct; oblique: 63.0% correct). The overall threshold for each lip was calculated with the constraints set at y0 = 33.33 and a = 66.66 (i.e. function fit between 33.33% and 66.66% correct performance). For data that did not converge into a four-parameter sigmoid function, threshold was determined by interpolation between groove widths that corresponded to just above and below the criterion (vertical: 65.5% correct; horizontal: 71.5% correct; oblique: 63.0% correct). Group data are presented in the text as mean ± standard deviation (SD) and in figures as mean ± standard error of the mean. Group response bias (experiment two) was analysed with one-way
1595
repeated measures analysis of variance (RM ANOVA) for comparison of response (%) in each orientation (vertical, horizontal, oblique). Group threshold data (experiment one) was analysed with two-way repeated measures ANOVA for comparison between lips (upper and lower) and grating orientation (horizontal, vertical, and oblique) (Sigmastat, 3.11, Systat Software Inc, Point Richmond, USA). A paired t-test was used for comparison of the overall threshold on the upper and lower lip. Statistical significance was set at 5%. 3. Results 3.1. Response bias Response bias within the three-alternative, forced-choice grating orientation protocol was assessed with application of a smooth polished Perspex probe whilst the volunteer was blindfolded (experiment two). On average, volunteers answered vertical in 31 ± 12% of trials, horizontal in 43 ± 15% of trials, and oblique in 26 ± 10% of trials. The percent response differed significantly between orientations (P = 0.03). Volunteers answered horizontal significantly more than oblique (P = 0.026) and volunteers tended to answer horizontal more than vertical (P = 0.07). Thus, the threshold criterion was set at 65.5% for the vertical orientation, 71.5% for the horizontal orientation, and 63.0% for the oblique orientation. 3.2. Threshold The average r2 for determination of threshold on the upper and lower lip was 0.85 ± 0.08 and 0.87 ± 0.05, respectively. The average r2 for determination of threshold in the vertical, horizontal, and oblique orientations was 0.72 ± 0.19, 0.62 ± 0.10, and 0.76 ± 0.09, respectively. There were seven instances (of a possible 78) where one of the orientations did not converge into a four-parameter sigmoid function. In these cases, threshold was determined by interpolation between the groove widths that corresponded to just above and below the threshold criterion for that orientation. The average overall threshold on the upper lip (1.5 ± 0.9 mm) was significantly greater than on the lower lip (1.0 ± 0.7 mm; paired t-test, P = 0.006). There was no significant main effect of orientation or lip on threshold and there was no significant orientation-by-lip interaction (Fig. 3).
100
Correct responses (%)
4. Discussion 80
The aim of the current study was to investigate anisotropy on the glabrous skin of human lips. The results demonstrate that spatial tactile acuity is greater on the lower lip than on the upper lip and anisotropy is absent at the midline.
H V O
60
4.1. Spatial tactile acuity
40
20
Horizontal Vertical Oblique
0 0.1
1
10
Grating width (mm) Fig. 2. Single subject data from experiment one showing the percentage of correct responses for each orientation as a function of the log grating width (mm). Data for the horizontal (circle), vertical (triangle), and oblique (square) orientations are fitted with a four-parameter sigmoid function (see Section 2). Long dash, horizontal function. Short dash, vertical function. Dotted line, oblique function. The group threshold estimate was 65.5%, 71.5%, and 63.0% for the vertical (V), horizontal (H), and oblique (O) orientations, respectively (based on the response bias measured in experiment two). The group threshold estimate for each orientation is marked on the y-axis.
Spatial tactile acuity and anisotropy was investigated at the midline of the upper and lower lip due to bilateral overlap of peripheral nerves in this region. Overlap of peripheral nerves at the midline is likely to increase the density of mechanoreceptive afferents and thus the total number of neurons responding to a particular stimulus. Enhanced acuity at midline structures has been reported for the lips, oral mucosa, tongue, and skin on the back when tested with two-point discrimination (Ringel and Ewanowski, 1965; Lass et al., 1972; Fuchs and Brown, 1984; Rath and Essick, 1990). At the midline, the average threshold on the lower lip (1.0 ± 0.7 mm) was significantly less than on the upper lip (1.5 ± 0.9 mm). This suggests that spatial tactile acuity was greater on the lower lip than on the upper lip. Enhanced spatial tactile acu-
A
B
100
80 H V O
60
40
Horizontal Vertical Oblique
20
0 0.1
1
10
Average lower lip correct responses (%)
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
Average upper lip correct responses (%)
1596
100
80
60
40
0 0.1
0.8
0.4
0
10
1.6
Average lower lip threshold (mm)
Average upper lip threshold (mm)
1.2
1
Grating width (mm)
D
1.6
Horizontal Vertical Oblique
20
Grating width (mm)
C
H V O
1.2
0.8
0.4
0 Vertical
Horizontal
Oblique
Orientation
Vertical
Horizontal
Oblique
Orientation
Fig. 3. Group data for experiment one showing the percentage of correct responses and threshold for each orientation on the upper and lower lip. Percentage of correct responses for each orientation is shown as a function of the log grating width (mm) for the upper lip (A) and lower lip (B). Data for the horizontal (circle), vertical (triangle), and oblique (square) orientations are fitted with a four-parameter sigmoid function (see Section 2). Long dash, horizontal function. Short dash, vertical function. Dotted line, oblique function. The threshold estimate was 65.5%, 71.5%, and 63.0% for the vertical, horizontal, and oblique orientations, respectively (based on the response bias measured in experiment two). The threshold estimate for each orientation is marked on the y-axis. The average threshold for each orientation is shown for the upper lip (C) and lower lip (D).
ity has also been observed on the lower lip (non-midline) with a two-choice grating orientation task (Patel et al., 1997; c.f. Wohlert, 1996). The difference in spatial tactile acuity between lips is most likely due to differences in innervation. The upper lip is innervated by the infraorbital nerve whereas the lower lip is innervated by the mental nerve. Regional differences in the type and density of mechanoreceptors or differences in the processing of afferent signals from the lips in the somatosensory cortex could also contribute. However, regional differences in the type and density of receptors on the lips has not been investigated and variation in the representation of lip regions on the somatosensory cortex is unlikely based on microelectrode recordings in Macaques (Nelson et al., 1980). 4.2. Anisotropy Investigation of anisotropy requires careful consideration of response bias. Gibson and Craig (2005) assessed response bias by calculating the ‘hit and false alarm’ rates for each orientation in a three-choice grating orientation task on the finger pad. The proportion of correct responses was then corrected for response bias for each orientation separately prior to determination of threshold. Using this approach, the authors confirmed the presence of anisotropy on the finger pad and at the base of the finger (Gibson and Craig, 2005). The presence of anisotropy on the finger confirmed the findings of an earlier study that used a two-choice grating orien-
tation task that assumed equal response bias between orientations and inferred equal response bias by comparing the percentage of correct responses for the two orientations at the smallest grating width (0.35 mm) (Vega-Bermudez and Johnson, 2004). In the current study, response bias was quantified in a largely independent group with the use of a smooth polished probe. Subjects were shown a probe with gratings and told that the gratings would be applied to the lip in three orientations. Subjects were then blindfolded and the smooth polished probe was applied to the lip instead of the probe with gratings. The results of the current study indicate that response bias is not equal between orientations. Volunteers answered horizontal (43 ± 15% of trials) significantly more than oblique (26 ± 10% of trials) and volunteers tended to answer horizontal more than vertical (31 ± 12% of trials). Thus, in the current study threshold was set separately for each orientation. When response bias was taken into account, there was no significant difference in threshold for the horizontal, vertical, and oblique orientations. This suggests that anisotropy is absent at the midline on human lips. Earlier reports of anisotropy on the lips are likely due to use of a two-choice grating orientation task, lack of measurement of response bias (Wohlert, 1996), or assumed equal response bias between orientations (Patel et al., 1997). The lack of anisotropy on the lips is surprising given that anisotropy is present on the finger and the finger and lips share similarities in sensation. On the finger pad and at the base of the index finger, acuity is greatest in the proximal–distal orientation (along
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
the axis of the finger) (Essock et al., 1992; Gibson and Craig, 2005). This orientation is parallel to the skin ridges and has the greatest skin compliance. The size and shape of receptive fields (Stevens and Patterson, 1995) and orientation-selective neurones in somatosensory cortex (Essock et al., 1992, 1997) have also been proposed as potential mechanisms for tactile anisotropy in the finger. Measurements of skin compliance and skin ridge orientation on human lips are not available. However, mechanoreceptor afferents that supply human lips exhibit similar characteristics to those of the hand. There are slowly adapting (SA) afferents on lips that resemble SA I afferents in hairy and glabrous skin of the hand. These afferents exhibit a high dynamic sensitivity and an irregular discharge during tissue deformation. There are also SA afferents on lips that resemble SA II afferents in the hand. These afferents exhibit spontaneous activity, a regular discharge rate, and a high sensitivity to lateral skin stretch (for review see Trulsson and Johansson, 2002). It is also worth noting that anisotropy is not limited to the somatosensory system. Anisotropy is also present in the human visual system. Visual acuity is greater when lines and edges are orientated horizontally or vertically as opposed to obliquely. Visual anisotropy is thought to be due to a greater proportion of cells that are selectively tuned to horizontal and vertical orientations rather than oblique orientations (for review see Appelle, 1972). The use of a grating orientation task to assess anisotropy and spatial tactile acuity on the lips is superior to that of two-point discrimination and gap detection for several reasons. First, the overall dimensions, edge contact, and contact area of the probe is similar regardless of the grating orientation thus eliminating non-spatial cues. Second, the threshold for a grating orientation task at the finger tip corresponds to the mean center-to-center spacing between slowly adapting afferent fibres in primate (macaque; 1.3 mm) and human skin (1.4 mm) (Johansson and Vallbo, 1979; DarianSmith and Kenins, 1980). Third, threshold measured with the grating orientation task is consistent with that obtained with more complex stimuli such as letters and Braille characters. Lastly, the underlying mechanisms for acuity in the grating orientation task are better understood than for two-point discrimination. Even so, there is a possible limitation to the use of the grating orientation task on the lips. The surface area of the upper and lower lip differs as does the surface area at the midline and the side of the lip. Thus, the proportion of glabrous and non-glabrous skin activated by the probe may differ between lip positions. Glabrous skin has greater acuity for two-point discrimination than non-glabrous skin (on the upper lip) possibly due to an increased density of mechanoreceptive afferents and smaller receptive field size for slowly adapting afferent fibres (Chen et al., 1995). The use of smaller grating probes may resolve this issue in future studies. Other points to consider when using a grating orientation task are that threshold increases with age, women tend to have a lower threshold than men (Wohlert, 1996; c.f. Patel et al., 1997), and threshold can improve by 2% between sessions (Van Boven and Johnson, 1994a). In summary, the results of the current study demonstrate that spatial tactile acuity is greater on the lower lip than on the upper lip and that anisotropy is absent on human lips. The greater spatial tactile acuity on the lower lip has implications for speech pathologists and clinicians. Although speech can be accomplished with limited auditory or tactile input (e.g. Kelso and Tuller, 1983), afferent input is required for adaptation to lip perturbation (Abbs and Gracco, 1984) and the formation of speech motor programs (e.g. Gracco and Abbs, 1985). This fits with the common experience that speech is often slurred when the lips are anaesthetised during dental treatment. The results of the current study suggest that sensation on the lower lip may be more important for speech than sensation on the upper lip. Tests of spatial tactile acuity have also been used to monitor recovery of sensation in patients with nerve damage resulting from trauma or elective jaw surgery
1597
(Van Boven and Johnson, 1994b). The results of the current study suggest that monitoring spatial tactile acuity over time requires determination of response bias and application of a constant set of orientations. Acknowledgements The author holds an Australian National Health and Medical Research Council Career Development Award. The author wishes to thank Ms. Heather J. Jarred, Mr. Peter D.F. Varacalli, Ms. Stefanie Heigele, and Mr. Benjamin D. Noll for assisting with collection of pilot data and Prof. Timothy S. Miles for advice during manuscript preparation. References Abbs JH, Gracco VL. Control of complex motor gestures: orofacial muscle responses to load perturbations of lip during speech. J Neurophysiol 1984;51:705–23. Appelle S. Perception and discrimination as a function of stimulus orientation: the ‘‘oblique effect’’ in man and animals. Psychol Bull 1972;78:266–78. Chen CC, Essick GK, Kelly DG, Young MG, Nestor JM, Masse B. Gender-, side- and site-dependent variations in human perioral spatial resolution. Arch Oral Biol 1995;40:539–48. Craig JC. Grating orientation as a measure of tactile spatial acuity. Somatosens Mot Res 1999;16:197–206. Darian-Smith I, Kenins P. Innervation density of mechanoreceptive fibres supplying glabrous skin of the monkey’s index finger. J Physiol 1980;309:147–55. Dreyer DA, Loe PR, Metz CB, Whitsel BL. Representation of head and face in postcentral gyrus of the macaque. J Neurophysiol 1975;38:714–33. Essock EA, Krebs WK, Prather JR. An anisotropy of human tactile sensitivity and its relation to the visual oblique effect. Exp Brain Res 1992;91:520–4. Essock EA, Krebs WK, Prather JR. Superior sensitivity for tactile stimuli orientated proximally-distally on the finger: implications for mixed Class 1 and Class 2 anisotropies. J Exp Psychol Hum Percept Perform 1997;23:515–27. Fuchs JL, Brown PB. Two-point discriminability: relation to properties of the somatosensory system. Somatosens Res 1984;2:163–9. Gibson GO, Craig JC. Tactile spatial sensitivity and anisotropy. Percept Psychophys 2005;67:1061–79. Gracco VL, Abbs JH. Dynamic control of the perioral system during speech: kinematic analyses of autogenic and nonautogenic sensorimotor processes. J Neurophysiol 1985;54:418–32. Grant AC, Fernandez R, Shilian P, Yanni E, Hill MA. Tactile spatial acuity differs between fingers: a study comparing two testing paradigms. Percept Psychophys 2006;68:1359–62. Green BG. The perception of distance and location for dual tactile pressures. Percept Psychophys 1982;31:315–23. Halata Z, Munger BL. The sensory innervation of primate facial skin. II. Vermilion border and mucosa of lip. Brain Res 1983;286:81–107. Hwang K, Suh MS, Chung IH. Cutaneous distribution of infraorbital nerve. J Craniofac Surg 2004;15:3–5. Johansson RS, Vallbo AB. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 1979;286:283–300. Johnson KO, Phillips JR. Tactile spatial resolution. I. Two-point discrimination, gap detection, grating resolution, and letter recognition. J Neurophysiol 1981;46:1177–92. Kelso JA, Tuller B. ‘‘Compensatory articulation’’ under conditions of reduced afferent information: a dynamic formulation. J Speech Hear Res 1983;26:217–24. Lass NJ, Kotchek CL, Deem JF. Oral two-point discrimination: further evidence of asymmetry on right and left sides of selected oral structures. Percept Mot Skills 1972;35:59–67. Lechelt EC. Spatial asymmetries in tactile discrimination of line orientation: a comparison of the sighted, visually impaired, and blind. Perception 1988;17:579–85. Nelson RJ, Sur M, Felleman DJ, Kaas JH. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J Comp Neurol 1980;192:611–43. Patel J, Essick GK, Kelly DG. Utility of square-wave gratings to assess perioral spatial acuity. J Oral Maxillofac Surg 1997;55:593–601. Phillips JR, Johnson KO. Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. J Neurophysiol 1981;46:1192–203. Rath EM, Essick GK. Perioral somesthetic sensibility: do the skin of the lower face and the midface exhibit comparable sensitivity? J Oral Maxillofac Surg 1990;48:1181–90. Ringel RL, Ewanowski SJ. Oral perception. I. Two-point discrimination. J Speech Hear Res 1965;8:389–98. Sathian K, Zangaladze A. Tactile spatial acuity at the human fingertip and lip: bilateral symmetry and interdigit variability. Neurology 1996;46:1464–6. Stevens JC, Patterson MQ. Dimensions of spatial acuity in the touch sense: changes over the life span. Somatosens Mot Res 1995;12:29–47.
1598
G. Todd / Clinical Neurophysiology 123 (2012) 1593–1598
Trulsson M, Johansson RS. Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors. Behav Brain Res 2002;135:27–33. Van Boven RW, Johnson KO. The limit of tactile spatial resolution in humans: grating orientation discrimination at the lip, tongue, and finger. Neurology 1994a;44:2361–6. Van Boven RW, Johnson KO. A psychophysical study of the mechanisms of sensory recovery following nerve injury in humans. Brain 1994b;117:149–67. Vega-Bermudez F, Johnson KO. Differences in spatial acuity between digits. Neurology 2001;56:1389–91.
Vega-Bermudez F, Johnson KO. Fingertip skin conformance accounts, in part, for differences in tactile spatial acuity in young subjects, but not for the decline in spatial acuity with aging. Percept Psychophys 2004;66:60–7. Wheat HE, Goodwin AW. Tactile discrimination of gaps by slowly adapting afferents: effects of population parameters and anisotropy in the fingerpad. J Neurophysiol 2000;84:1430–44. Wohlert AB. Tactile perception of spatial stimuli on the lip surface by young and older adults. J Speech Hear Res 1996;39:1191–8. Wong TS, Ho R, Ho J. Influence of shape of receptor organ on the horizontal–vertical illusion in passive touch. J Exp Psychol 1974;103:414–9.