G Model NSL-32366; No. of Pages 6
ARTICLE IN PRESS Neuroscience Letters xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Laterality of proprioception in the orofacial muscles and temporomandibular joint Ellie Frayne a,∗ , Dr. Susan Coulson a , Dr. Roger Adams a , Glen Croxson (A/Prof.) b , Prof. Gordon Waddington c a
University of Sydney, Faculty of Health Sciences Cumberland Campus, 75 East St., Lidcombe, Sydney, NSW 2141, Australia University of Sydney, Faculty of Medicine, Central Clinical School, RPA Hospital, Missenden Road, Camperdown, NSW, Australia c University of Canberra, Building 12 D, University of Canberra, ACT 2600, Australia b
h i g h l i g h t s • • • •
Closure movement proprioception is better at lips than jaw. Lip and jaw proprioceptive acuity are correlated on the right side but not on the left. Right side lips had higher discrimination acuity than left only for small objects. Findings consistent with use-based proprioception enhancement and matching for coordinated function.
a r t i c l e
i n f o
Article history: Received 3 June 2016 Received in revised form 5 September 2016 Accepted 18 October 2016 Available online xxx Keywords: Proprioception Face Facial paralysis Bell’s palsy Laterality Cerebral dominance
a b s t r a c t Laterality of function in the orofacial musculature suggests there may be side-to-side asymmetry of proprioceptive acuity in lip movement compared to the temporomandibular joint (TMJ). In the present work, 14 young adults were tested for acuity of lip and TMJ closure movements onto plugs varying from 5 to 8 mm without visual feedback. Testing was conducted on both left and right sides, using the same psychophysical task and stimuli. Results showed superior proprioceptive acuity at the lips, with no significant side effect. However, there was side-to-side asymmetry in the correlations between proprioceptive performance for the two anatomical structures, with performance on the right side strongly correlated but not on the left. This is consistent with the need for coordination between structures during chewing. When acuity at different points in the stimulus range was examined, the right side lips were better with small stimuli. Overall, results support enhanced use-specific proprioception. © 2016 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Laterality in the neurotypical, healthy face has been demonstrated with respect to two-point discrimination and range of motion during facial expression [6,11]. However, it is not currently known as to whether laterality is also apparent in the control of orofacial movement. The control of emotion, speech and proprioception has been linked to cerebral dominance. Specifically, in right-handers, speech is predominantly lateralized to the left hemisphere [10] and proprioception to the right hemisphere [20] and lower-limb proprioception is better on the non-dominant left side [25]. Thus there may be lateralization in the facial expression of
∗ Corresponding author. E-mail address: [email protected] (E. Frayne).
emotion, as well as the conscious and subconscious control of the orofacial muscles. However, such lateral asymmetry has not been examined with respect to proprioceptive performance in facial structures. If “facedness” is present in orofacial structures, it could have clinical implications for whether or not visual feedback is the primary modality used for rehabilitation exercises, dependent on which side of the face or temporomandibular joint (TMJ) is affected. Additionally, laterality in facial and TMJ proprioception may support current theories of contralateral hemispheric control of non-preferred side proprioception [21]. Proprioception is a complex sensation involving the peripheral and central processing of information regarding position sense at rest (position sense) and during movement (kinaesthesia) that arises from peripheral mechanoreceptors and is centrally processed to match with a pre stored body map or schema of the body [5,17,19,22,23]. Proprioception is often researched in the context
http://dx.doi.org/10.1016/j.neulet.2016.10.030 0304-3940/© 2016 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
G Model NSL-32366; No. of Pages 6 2
ARTICLE IN PRESS E. Frayne et al. / Neuroscience Letters xxx (2016) xxx–xxx
of injury rehabilitation and prevention in general musculoskeletal physiotherapy [36,38,44,47]. In relation to the face, knowledge of proprioception in a neurotypical population would aid in the prescription of exercises reliant on proprioceptive acuity, where these are used for people recovering from facial nerve paralysis, embouchure dystonia, facial injury or TMJ disorder. Deficits involving proprioception can be observed following various facial and TMJ injuries. For example, following facial nerve paralysis, there is a lack in synchronous movement at the mouth [13], and embouchure dystonia indicates a pathological overactivity of the lip sensory-motor system and involves involuntary contraction of the lips that is often seen in musicians [16,30]. Additionally, following Bell’s palsy, altered sensation is reported without any clear sensory deficit [45]. It has been speculated that this disordered information is due to altered proprioception, as opposed to sensation as both travel along that same afferent pathways. In the TMJ, proprioception can be affected by TMJ disorder (TMD) [1], ankylosis [32], or hypermobility [9]. Interestingly, strong preference in chewing side has been linked to increased risk of TMD and to osseous changes in the TMJ in asymptomatic people [33,40,42]. Investigation into normal facial movement and sensation has shown that, independent of handedness, the left side of the face moves through more range of motion and is more involved in emotional expression than the right [12]. It has also been noted that two-point discrimination thresholds are lower on the left side of the face independent of gender [6], and that the threshold of discrimination for lateral movements of the mandible is lower on the left than on the right [51]. These findings would suggest a left side proprioceptive superiority. The focus of the current research was to investigate the motor control of the orofacial muscles and to determine whether there is a lateral asymmetry in proprioceptive acuity, in a manner similar to that observed in the upper and lower limbs [25,27] and eyes [7]. Recent research into the comparative proprioceptive acuity of the lips and TMJ when tested at the centre point has indicated greater acuity at the lips relative to the TMJ on the same psychophysical discrimination task despite a distinct lack of traditional proprioceptors (muscle spindles and Golgi tendon organs) in the facial musculature [15]. Importantly, the proprioceptive discrimination scores at the lips were found to correlate to the TMJ acuity scores, and it was hypothesised that this relationship could be explained by the extensive co-ordinated use of the lips and TMJ complex [15]. Improved proprioception due to extensive use has been documented across the body including in the ankle [4] and neck [24] and elite athletes have been found to have greater proprioceptive ability at sport relevant joints [26,29]. The unique usage of the orofacial muscles in facial expression; speech and mastication would imply complex cortical control as the orofacial muscles are subject to emotional control, volitional control and reflexive control. The cortical control areas for the motor control of emotional or volitional speech differ from those relating to emotional or volitional facial expression [8,31] thus it is unknown if cerebral dominance effects would be present in the orofacial muscles or if laterality could be related to extensive asymmetric use of the facial muscles. Given extensive use in an asymmetric fashion, investigation for lateral asymmetry in proprioception seems warranted. The aim of this study is to determine whether or not laterality is present in the orofacial muscles in comparison to the TMJ when tested on the same psychophysical distance discrimination task. The asymmetry of movement at the mouth and previous proprioceptive work conducted at the midline lead to the hypothesis that the left side of the lips would have the greatest proprioceptive acuity, followed by the right lips and then the left and right TMJ. Laterality of proprioception has been identified in other research on the upper and lower limbs, with the non-dominant side found to have better proprioceptive acuity, and this has implications for rehabilitation exercises
as it has been determined that dominant limb control relies more on visual feedback, and the non dominant side on proprioception [18,19,25,27]. If lateral asymmetry is seen in the movement discrimination ability of the lower face or TMJ, it could alter how these areas are rehabilitated, with or without visual feedback, given that typical rehabilitation programs for both areas involve the use of mirror biofeedback [3,14]. 2. Materials and methods 2.1. Participants Fourteen healthy volunteers between the ages of 18 and 65 (male 4 female 10; mean age 25.6 SD 3.9) were recruited from advertisements placed on notice boards at the University of Sydney Health Sciences campus. All potential participants were screened for facial, TMJ or dental injuries and disorders; facial nerve damage; significant lower facial deformities (e.g. cleft palate) and significant recent dental work. They were also screened for diagnosis of conditions that could significantly affect proprioception including: 1) neurological conditions (multiple sclerosis, Parkinson’s disease, chronic fatigue syndrome) 2) recent heart failure 3) Type 1 or 2 diabetes 4) vestibular disturbances such as benign paroxysmal positional vertigo 5) rheumatoid arthritis. All volunteers had no chronic conditions and had no specific intensive motor control training involving the mouth or lips, such as from playing a musical instrument. The project was approved by the University of Sydney Ethics Committee (2014/641). 2.2. Design Participants completed a repeated measures study involving two equivalent discrimination tasks, for both the lips and TMJ, tested on either side of the mouth. 2.3. Apparatus A specific active movement extent discrimination apparatus (AMEDA) for the lips and TMJ was used. This apparatus was developed from dental research work [52] and was used to conduct the first test of lip versus TMJ proprioception, using a task at the midline of the mouth [15]. In the present study, discrimination ability of lip closure movements and TMJ closure movements on either side of the mouth were compared using this apparatus. Four differently-sized cylindrical plastic plugs, with 1 mm diameter stepped differences, were used. The plug circumference was checked using Mitutoyo digital callipers (IP67 ABS Coolant Proof Calliper) to ensure a 1 mm step between each stimulus, as specified by the manufacturer. A 33.5 mm diameter plastic plug was used to create the standardised starting position for each trial at both the lips and TMJ (Fig. 1). The disposable plastic plugs and starting piece were attached to thin rods to enable ease of pre-use disinfection and presentation to the mouth. To maximise the ecological validity of the test, participants were not restrained or blindfolded, although vision of the test piece was shielded [28]. The psychophysical method employed has been previously used in assessing proprioceptive ability in the upper and lower limbs, lower back, neck and TMJ, and met the validity criteria and number of trials needed to accurately estimate active movement discrimination ability [2,26]. 2.4. Procedures All the apparatus was sterilised using Milton solution and was stored in labelled zip-lock bags. Participants were screened for
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
G Model NSL-32366; No. of Pages 6
ARTICLE IN PRESS E. Frayne et al. / Neuroscience Letters xxx (2016) xxx–xxx
3
Fig. 1. AMEDA Lip and Jaw. Panel 1 (left) starting piece AMEDA TMJ; Panel 2 TMJ test plug; Panel 3 (middle right) starting piece lips; Panel 4 (right) lip test piece.
allergies relating to Milton prior to participating. During assembly, researchers handled the stimulus plugs with gloves. Maximum TMJ opening was recorded per participant to ensure the starting point was within comfortable range. Participants were tested for handedness using the Edinburgh handedness scale prior to commencing testing [29,50], and asked about side preference for chewing. During testing, participants were seated, resting their elbows on the table in front of them and holding a cardboard shield under their nose, thus stabilising the head and upper limbs, and obscuring vision of the stimuli to ensure that test results were solely due to proprioception. Testing involved 4 conditions, right jaw, right lips, left jaw and left lips, and the sequence of conditions was alternated according to a Latin square. Overall, four sets of 40 stimuli were presented in a random sequence, with each stimulus presented 10 times in each condition to ensure valid discrimination acuity measures could be calculated [34]. A short rest was given before the each subsequent AMEDA condition commenced. The testing procedure involved placing the starting piece, as seen in Fig. 1, between the lips or teeth at the midline, where participants were asked to ‘hold’ the start piece, after which it was quickly removed and replaced on the side of the mouth with one of 4 test pieces (plugs ranging from 5 to 8 mm in diameter) following a predetermined random sequence. Thereafter, when the stimulus had been placed between the maxillary lateral incisor and the maxillary cuspid (canine) for jaw test conditions, a closure movement was made. For lip testing, the stimulus was placed at the same point, but held further out so that only the lips would touch it upon closure. Participants were then asked to respond with one of 4 number options reflecting their judgement. The longest movement was called “1” (5 mm stimulus, 28.5 mm movement) and the shortest was named “4” (the largest stimulus 8 mm, 25.5 mm movement). Participants were given a familiarisation session consisting of two presentations of each stimulus size, once in order of size, then once in random presentation order. For testing the lips, participants were instructed to make a movement as they would when closing their lips onto a drinking straw. This familiarisation sequence was repeated with the TMJ, with instructions that included gently closing the teeth to contact onto the start piece and, following its removal, to move to contact the stimulus. 2.5. Data analysis Data analysis was performed using SPSS (version 22), with a p value of 0.05 chosen to indicate statistical significance. Non-parametric signal detection analysis was used to produce pair-wise receiver operating characteristic curves (ROC curves),
then a pair-wise area under the curve (AUC) was calculated to reflect each participant’s ability to discriminate between stimulus pairs 1–2, 2–3, 3–4 and 1–4 on the left and right sides of their mouth, as well as determine their overall proprioceptive ability at the lips and the TMJ. The mean AUC per person was recorded as the average of the 1–2, 2–3, 3–4 pairings, thus giving each participant single movement discrimination scores for either side of the lips, and for either side of the TMJ. The AUC statistic is a non-biased discrimination measure based on signal detection theory [37,46]. An AUC score of 0.5 indicates that two stimuli would be judged as the same, i.e. Judgment would be due to chance, with a score of 1.0 being perfect discrimination ability. Repeated measures analysis of variance (ANOVA) was used to compare the data from the lips and TMJ and to determine if there was any difference in ability between the two anatomical structures and between sides. To determine whether the proprioceptive ability of the left and right sides and the lip and TMJ were related to each other, Pearson’s correlations were calculated. A factorial repeated measures ANOVA, with factors; Structure (Lips, TMJ), Side (left, right) and Stimulus Pair (1 vs 2, 2 vs 3, 3 vs 4) was used to determine the effect of these factors on AUC scores. Polynomial trend analysis was carried out to examine for trends with increasing size of Stimulus Pair. 3. Results Thirteen of the fourteen participants were right-handed. Six reported that they chewed on the right side of their mouth, and eight participants could not report a preferred chewing side. ANOVA results for the main effects indicated that, for the Structure factor, the lips showed significantly greater proprioceptive acuity (mean AUC = 0.86) compared to the TMJ (0.80) on the same psychophysical task (F 1,13 = 17.90, p = 0.001, 2 p = 0.579), while there was no significant difference between overall proprioceptive acuity on the right side (mean AUC = 0.84) and on the left side (0.82) with F 1,13 = 1.25, p = 0.284, 2 p = 0.088. The interaction between these factors was not significant (p = 0.97). No significant linear trend was found as stimulus pair values increased (F 1,13 = 0.49, p = 0.496, 2 p = 0.036), however there was a significant quadratic relationship (F 1,13 = 9.65, p = 0.008, 2 p = 0.426), reflecting better discrimination for the extreme stimulus pair values than for the middle stimulus pair (see Fig. 2a and b). No interaction involving structure and side and the linear or quadratic trend components was significant (all p > 0.086) (Fig. 3). When t-tests were conducted to examine the side-to-side differences at different Stimulus pair values for the two structures, only the difference at the smallest size stimulus pair between the
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
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E. Frayne et al. / Neuroscience Letters xxx (2016) xxx–xxx
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Fig. 2. a) Right side mean pairwise AUCs. b) Left side mean pairwise AUCs.
Table 1 Correlations between Lip and Jaw AUC at different locations and Left and Right AUCs. Values for p are in brackets. Lip Jaw Centre correlation is from Frayne et al. [15]. Lip-Jaw Left
Lip-Jaw Centre
Lip-Jaw Right
Lip-Jaw overall
Left-Right Lips
Left-Right Jaw
Left-Right overall
−0.04 (0.89)
0.51 (0.02)
0.75 (0.002)
0.36 (0.22)
0.14 (0.63)
0.14 (0.63)
0.04 (0.89)
Table 2 Mean Error in mm for the lips and Jaw, on the right and left sides. Stimulus
Discrimination ability (mm)
SD
95% CI
Right Lips Left Lips Right Jaw Left Jaw
0.24 0.28 0.39 0.40
0.10 0.11 0.28 0.13
0.1831–0.2997 0.2266–0.5484 0.2197–0.3445 0.3255–0.4781
SD: standard deviation; CI 95% confidence interval.
right side lips (mean AUC = 0.90) and the left (0.83) was significant (t 13 = 2.42, p = 0.03), with all other p > 0.15. Conversely, while no significant difference was found between the performance of the right lips (mean AUC = 0.87) and right jaw (0.86) at the largest stimulus pair 3–4 (p = 0.63) all other lip vs. jaw pair comparisons had p values
ARTICLE IN PRESS Neuroscience Letters xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Laterality of proprioception in the orofacial muscles and temporomandibular joint Ellie Frayne a,∗ , Dr. Susan Coulson a , Dr. Roger Adams a , Glen Croxson (A/Prof.) b , Prof. Gordon Waddington c a
University of Sydney, Faculty of Health Sciences Cumberland Campus, 75 East St., Lidcombe, Sydney, NSW 2141, Australia University of Sydney, Faculty of Medicine, Central Clinical School, RPA Hospital, Missenden Road, Camperdown, NSW, Australia c University of Canberra, Building 12 D, University of Canberra, ACT 2600, Australia b
h i g h l i g h t s • • • •
Closure movement proprioception is better at lips than jaw. Lip and jaw proprioceptive acuity are correlated on the right side but not on the left. Right side lips had higher discrimination acuity than left only for small objects. Findings consistent with use-based proprioception enhancement and matching for coordinated function.
a r t i c l e
i n f o
Article history: Received 3 June 2016 Received in revised form 5 September 2016 Accepted 18 October 2016 Available online xxx Keywords: Proprioception Face Facial paralysis Bell’s palsy Laterality Cerebral dominance
a b s t r a c t Laterality of function in the orofacial musculature suggests there may be side-to-side asymmetry of proprioceptive acuity in lip movement compared to the temporomandibular joint (TMJ). In the present work, 14 young adults were tested for acuity of lip and TMJ closure movements onto plugs varying from 5 to 8 mm without visual feedback. Testing was conducted on both left and right sides, using the same psychophysical task and stimuli. Results showed superior proprioceptive acuity at the lips, with no significant side effect. However, there was side-to-side asymmetry in the correlations between proprioceptive performance for the two anatomical structures, with performance on the right side strongly correlated but not on the left. This is consistent with the need for coordination between structures during chewing. When acuity at different points in the stimulus range was examined, the right side lips were better with small stimuli. Overall, results support enhanced use-specific proprioception. © 2016 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Laterality in the neurotypical, healthy face has been demonstrated with respect to two-point discrimination and range of motion during facial expression [6,11]. However, it is not currently known as to whether laterality is also apparent in the control of orofacial movement. The control of emotion, speech and proprioception has been linked to cerebral dominance. Specifically, in right-handers, speech is predominantly lateralized to the left hemisphere [10] and proprioception to the right hemisphere [20] and lower-limb proprioception is better on the non-dominant left side [25]. Thus there may be lateralization in the facial expression of
∗ Corresponding author. E-mail address: [email protected] (E. Frayne).
emotion, as well as the conscious and subconscious control of the orofacial muscles. However, such lateral asymmetry has not been examined with respect to proprioceptive performance in facial structures. If “facedness” is present in orofacial structures, it could have clinical implications for whether or not visual feedback is the primary modality used for rehabilitation exercises, dependent on which side of the face or temporomandibular joint (TMJ) is affected. Additionally, laterality in facial and TMJ proprioception may support current theories of contralateral hemispheric control of non-preferred side proprioception [21]. Proprioception is a complex sensation involving the peripheral and central processing of information regarding position sense at rest (position sense) and during movement (kinaesthesia) that arises from peripheral mechanoreceptors and is centrally processed to match with a pre stored body map or schema of the body [5,17,19,22,23]. Proprioception is often researched in the context
http://dx.doi.org/10.1016/j.neulet.2016.10.030 0304-3940/© 2016 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
G Model NSL-32366; No. of Pages 6 2
ARTICLE IN PRESS E. Frayne et al. / Neuroscience Letters xxx (2016) xxx–xxx
of injury rehabilitation and prevention in general musculoskeletal physiotherapy [36,38,44,47]. In relation to the face, knowledge of proprioception in a neurotypical population would aid in the prescription of exercises reliant on proprioceptive acuity, where these are used for people recovering from facial nerve paralysis, embouchure dystonia, facial injury or TMJ disorder. Deficits involving proprioception can be observed following various facial and TMJ injuries. For example, following facial nerve paralysis, there is a lack in synchronous movement at the mouth [13], and embouchure dystonia indicates a pathological overactivity of the lip sensory-motor system and involves involuntary contraction of the lips that is often seen in musicians [16,30]. Additionally, following Bell’s palsy, altered sensation is reported without any clear sensory deficit [45]. It has been speculated that this disordered information is due to altered proprioception, as opposed to sensation as both travel along that same afferent pathways. In the TMJ, proprioception can be affected by TMJ disorder (TMD) [1], ankylosis [32], or hypermobility [9]. Interestingly, strong preference in chewing side has been linked to increased risk of TMD and to osseous changes in the TMJ in asymptomatic people [33,40,42]. Investigation into normal facial movement and sensation has shown that, independent of handedness, the left side of the face moves through more range of motion and is more involved in emotional expression than the right [12]. It has also been noted that two-point discrimination thresholds are lower on the left side of the face independent of gender [6], and that the threshold of discrimination for lateral movements of the mandible is lower on the left than on the right [51]. These findings would suggest a left side proprioceptive superiority. The focus of the current research was to investigate the motor control of the orofacial muscles and to determine whether there is a lateral asymmetry in proprioceptive acuity, in a manner similar to that observed in the upper and lower limbs [25,27] and eyes [7]. Recent research into the comparative proprioceptive acuity of the lips and TMJ when tested at the centre point has indicated greater acuity at the lips relative to the TMJ on the same psychophysical discrimination task despite a distinct lack of traditional proprioceptors (muscle spindles and Golgi tendon organs) in the facial musculature [15]. Importantly, the proprioceptive discrimination scores at the lips were found to correlate to the TMJ acuity scores, and it was hypothesised that this relationship could be explained by the extensive co-ordinated use of the lips and TMJ complex [15]. Improved proprioception due to extensive use has been documented across the body including in the ankle [4] and neck [24] and elite athletes have been found to have greater proprioceptive ability at sport relevant joints [26,29]. The unique usage of the orofacial muscles in facial expression; speech and mastication would imply complex cortical control as the orofacial muscles are subject to emotional control, volitional control and reflexive control. The cortical control areas for the motor control of emotional or volitional speech differ from those relating to emotional or volitional facial expression [8,31] thus it is unknown if cerebral dominance effects would be present in the orofacial muscles or if laterality could be related to extensive asymmetric use of the facial muscles. Given extensive use in an asymmetric fashion, investigation for lateral asymmetry in proprioception seems warranted. The aim of this study is to determine whether or not laterality is present in the orofacial muscles in comparison to the TMJ when tested on the same psychophysical distance discrimination task. The asymmetry of movement at the mouth and previous proprioceptive work conducted at the midline lead to the hypothesis that the left side of the lips would have the greatest proprioceptive acuity, followed by the right lips and then the left and right TMJ. Laterality of proprioception has been identified in other research on the upper and lower limbs, with the non-dominant side found to have better proprioceptive acuity, and this has implications for rehabilitation exercises
as it has been determined that dominant limb control relies more on visual feedback, and the non dominant side on proprioception [18,19,25,27]. If lateral asymmetry is seen in the movement discrimination ability of the lower face or TMJ, it could alter how these areas are rehabilitated, with or without visual feedback, given that typical rehabilitation programs for both areas involve the use of mirror biofeedback [3,14]. 2. Materials and methods 2.1. Participants Fourteen healthy volunteers between the ages of 18 and 65 (male 4 female 10; mean age 25.6 SD 3.9) were recruited from advertisements placed on notice boards at the University of Sydney Health Sciences campus. All potential participants were screened for facial, TMJ or dental injuries and disorders; facial nerve damage; significant lower facial deformities (e.g. cleft palate) and significant recent dental work. They were also screened for diagnosis of conditions that could significantly affect proprioception including: 1) neurological conditions (multiple sclerosis, Parkinson’s disease, chronic fatigue syndrome) 2) recent heart failure 3) Type 1 or 2 diabetes 4) vestibular disturbances such as benign paroxysmal positional vertigo 5) rheumatoid arthritis. All volunteers had no chronic conditions and had no specific intensive motor control training involving the mouth or lips, such as from playing a musical instrument. The project was approved by the University of Sydney Ethics Committee (2014/641). 2.2. Design Participants completed a repeated measures study involving two equivalent discrimination tasks, for both the lips and TMJ, tested on either side of the mouth. 2.3. Apparatus A specific active movement extent discrimination apparatus (AMEDA) for the lips and TMJ was used. This apparatus was developed from dental research work [52] and was used to conduct the first test of lip versus TMJ proprioception, using a task at the midline of the mouth [15]. In the present study, discrimination ability of lip closure movements and TMJ closure movements on either side of the mouth were compared using this apparatus. Four differently-sized cylindrical plastic plugs, with 1 mm diameter stepped differences, were used. The plug circumference was checked using Mitutoyo digital callipers (IP67 ABS Coolant Proof Calliper) to ensure a 1 mm step between each stimulus, as specified by the manufacturer. A 33.5 mm diameter plastic plug was used to create the standardised starting position for each trial at both the lips and TMJ (Fig. 1). The disposable plastic plugs and starting piece were attached to thin rods to enable ease of pre-use disinfection and presentation to the mouth. To maximise the ecological validity of the test, participants were not restrained or blindfolded, although vision of the test piece was shielded [28]. The psychophysical method employed has been previously used in assessing proprioceptive ability in the upper and lower limbs, lower back, neck and TMJ, and met the validity criteria and number of trials needed to accurately estimate active movement discrimination ability [2,26]. 2.4. Procedures All the apparatus was sterilised using Milton solution and was stored in labelled zip-lock bags. Participants were screened for
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
G Model NSL-32366; No. of Pages 6
ARTICLE IN PRESS E. Frayne et al. / Neuroscience Letters xxx (2016) xxx–xxx
3
Fig. 1. AMEDA Lip and Jaw. Panel 1 (left) starting piece AMEDA TMJ; Panel 2 TMJ test plug; Panel 3 (middle right) starting piece lips; Panel 4 (right) lip test piece.
allergies relating to Milton prior to participating. During assembly, researchers handled the stimulus plugs with gloves. Maximum TMJ opening was recorded per participant to ensure the starting point was within comfortable range. Participants were tested for handedness using the Edinburgh handedness scale prior to commencing testing [29,50], and asked about side preference for chewing. During testing, participants were seated, resting their elbows on the table in front of them and holding a cardboard shield under their nose, thus stabilising the head and upper limbs, and obscuring vision of the stimuli to ensure that test results were solely due to proprioception. Testing involved 4 conditions, right jaw, right lips, left jaw and left lips, and the sequence of conditions was alternated according to a Latin square. Overall, four sets of 40 stimuli were presented in a random sequence, with each stimulus presented 10 times in each condition to ensure valid discrimination acuity measures could be calculated [34]. A short rest was given before the each subsequent AMEDA condition commenced. The testing procedure involved placing the starting piece, as seen in Fig. 1, between the lips or teeth at the midline, where participants were asked to ‘hold’ the start piece, after which it was quickly removed and replaced on the side of the mouth with one of 4 test pieces (plugs ranging from 5 to 8 mm in diameter) following a predetermined random sequence. Thereafter, when the stimulus had been placed between the maxillary lateral incisor and the maxillary cuspid (canine) for jaw test conditions, a closure movement was made. For lip testing, the stimulus was placed at the same point, but held further out so that only the lips would touch it upon closure. Participants were then asked to respond with one of 4 number options reflecting their judgement. The longest movement was called “1” (5 mm stimulus, 28.5 mm movement) and the shortest was named “4” (the largest stimulus 8 mm, 25.5 mm movement). Participants were given a familiarisation session consisting of two presentations of each stimulus size, once in order of size, then once in random presentation order. For testing the lips, participants were instructed to make a movement as they would when closing their lips onto a drinking straw. This familiarisation sequence was repeated with the TMJ, with instructions that included gently closing the teeth to contact onto the start piece and, following its removal, to move to contact the stimulus. 2.5. Data analysis Data analysis was performed using SPSS (version 22), with a p value of 0.05 chosen to indicate statistical significance. Non-parametric signal detection analysis was used to produce pair-wise receiver operating characteristic curves (ROC curves),
then a pair-wise area under the curve (AUC) was calculated to reflect each participant’s ability to discriminate between stimulus pairs 1–2, 2–3, 3–4 and 1–4 on the left and right sides of their mouth, as well as determine their overall proprioceptive ability at the lips and the TMJ. The mean AUC per person was recorded as the average of the 1–2, 2–3, 3–4 pairings, thus giving each participant single movement discrimination scores for either side of the lips, and for either side of the TMJ. The AUC statistic is a non-biased discrimination measure based on signal detection theory [37,46]. An AUC score of 0.5 indicates that two stimuli would be judged as the same, i.e. Judgment would be due to chance, with a score of 1.0 being perfect discrimination ability. Repeated measures analysis of variance (ANOVA) was used to compare the data from the lips and TMJ and to determine if there was any difference in ability between the two anatomical structures and between sides. To determine whether the proprioceptive ability of the left and right sides and the lip and TMJ were related to each other, Pearson’s correlations were calculated. A factorial repeated measures ANOVA, with factors; Structure (Lips, TMJ), Side (left, right) and Stimulus Pair (1 vs 2, 2 vs 3, 3 vs 4) was used to determine the effect of these factors on AUC scores. Polynomial trend analysis was carried out to examine for trends with increasing size of Stimulus Pair. 3. Results Thirteen of the fourteen participants were right-handed. Six reported that they chewed on the right side of their mouth, and eight participants could not report a preferred chewing side. ANOVA results for the main effects indicated that, for the Structure factor, the lips showed significantly greater proprioceptive acuity (mean AUC = 0.86) compared to the TMJ (0.80) on the same psychophysical task (F 1,13 = 17.90, p = 0.001, 2 p = 0.579), while there was no significant difference between overall proprioceptive acuity on the right side (mean AUC = 0.84) and on the left side (0.82) with F 1,13 = 1.25, p = 0.284, 2 p = 0.088. The interaction between these factors was not significant (p = 0.97). No significant linear trend was found as stimulus pair values increased (F 1,13 = 0.49, p = 0.496, 2 p = 0.036), however there was a significant quadratic relationship (F 1,13 = 9.65, p = 0.008, 2 p = 0.426), reflecting better discrimination for the extreme stimulus pair values than for the middle stimulus pair (see Fig. 2a and b). No interaction involving structure and side and the linear or quadratic trend components was significant (all p > 0.086) (Fig. 3). When t-tests were conducted to examine the side-to-side differences at different Stimulus pair values for the two structures, only the difference at the smallest size stimulus pair between the
Please cite this article in press as: E. Frayne, et al., Laterality of proprioception in the orofacial muscles and temporomandibular joint, Neurosci. Lett. (2016), http://dx.doi.org/10.1016/j.neulet.2016.10.030
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Fig. 2. a) Right side mean pairwise AUCs. b) Left side mean pairwise AUCs.
Table 1 Correlations between Lip and Jaw AUC at different locations and Left and Right AUCs. Values for p are in brackets. Lip Jaw Centre correlation is from Frayne et al. [15]. Lip-Jaw Left
Lip-Jaw Centre
Lip-Jaw Right
Lip-Jaw overall
Left-Right Lips
Left-Right Jaw
Left-Right overall
−0.04 (0.89)
0.51 (0.02)
0.75 (0.002)
0.36 (0.22)
0.14 (0.63)
0.14 (0.63)
0.04 (0.89)
Table 2 Mean Error in mm for the lips and Jaw, on the right and left sides. Stimulus
Discrimination ability (mm)
SD
95% CI
Right Lips Left Lips Right Jaw Left Jaw
0.24 0.28 0.39 0.40
0.10 0.11 0.28 0.13
0.1831–0.2997 0.2266–0.5484 0.2197–0.3445 0.3255–0.4781
SD: standard deviation; CI 95% confidence interval.
right side lips (mean AUC = 0.90) and the left (0.83) was significant (t 13 = 2.42, p = 0.03), with all other p > 0.15. Conversely, while no significant difference was found between the performance of the right lips (mean AUC = 0.87) and right jaw (0.86) at the largest stimulus pair 3–4 (p = 0.63) all other lip vs. jaw pair comparisons had p values
