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Developmental and age-related changes in reflexes of the human jaw-closing system
Electroencephalograph), and clinical Neurophysiology, 1991, 81 : 118-128 © 1991 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/91/$03.50 ADONIS 0924980X9100065U
118
ELMOCO 89214
Developmental and age-related changes in reflexes of the human jaw-closing system Anne Smith, Christine M. Weber, Joann Newton and Margaret Denny Department of Audiology and Speech Sciences, Purdue University, West Lafayette, IN 47907 (U.S.A.)
(Accepted for publication: 25 June 1990)
Summary Reflex responses of the jaw-closing system to innocuous mechanical stimulation of the tongue and palate were examined in a group of 25 girls aged 7-8 years and in a group of 25 women aged 70-80 years. Responses were measured both as changes in background biting force and from bilateral recordings of masseter EMGs. For comparative purposes, results from an earlier study of 35 young adult women (aged 18-25 years) were available. Compared to younger groups of subjects, reflex responses of the elderly were reduced in numbers and amplitude, were characterized by fewer initial excitatory component responses, and had longer latency to onset. Analyses of responses of the children indicated that age 7-8 years is a transitional period. Some children show adult-like responses, while others display responses that appear to represent earlier forms or transitional responses. These results suggest that oral-motor reflexes are not fixed response patterns upon which more complex motor skills, such as speech, are built. Rather, oral reflex development appears to occur in concert with the acquisition of complex motor skills. Systematic changes in reflex responses also occur in the period from young adulthood to the seventh decade of life. This result indicates a continuous evolution of oral sensorimotor systems throughout the human life span. Key words: Jaw-closing system; Oral sensorimotor system; Reflex response; Mechanical stimulation; Developmental change; Age-related change
G r o w i n g awareness of the p o t e n t i a l significance of changes in reflex f u n c t i o n that m a y occur with d e v e l o p m e n t a n d aging has m o t i v a t e d n u m e r o u s investigations of stretch a n d c u t a n e o u s reflexes of the u p p e r a n d lower l i m b s in c h i l d r e n a n d elderly subjects (e.g., C l a r k s o n 1978; Bawa 1981; Issler a n d Stephens 1983; R o w l a n d son a n d Stephens 1985; H a r t 1986). T h e results of these investigations have significant i m p l i c a t i o n s for u n d e r s t a n d i n g d e v e l o p i n g m o t o r skills a n d m o t o r perform a n c e in the elderly. F u r t h e r m o r e , careful d e s c r i p t i o n s of h u m a n reflex f u n c t i o n are i m p o r t a n t clinically a n d to theories of m o t o r control, which often i n c o r p o r a t e the i d e a that m o r e c o m p l e x m o t o r b e h a v i o r s are b u i l t on a f o u n d a t i o n of pre-existing reflex circuitry (e.g., Berkinb l i t et al. 1986). I n c o n t r a s t to reflexes o f the limbs, p o s s i b l e changes in reflexes of the h u m a n o r a l - m o t o r system over the life s p a n have received little q u a n t i t a t i v e e x p e r i m e n t a l attention, a l t h o u g h the r e - e m e r g e n c e of ' p r i m i t i v e ' or ' d e v e l o p m e n t a l ' oral reflexes in aged p a t i e n t s has often b e e n d e s c r i b e d (e.g., P a u l s o n a n d G o t t l i e b 1968). This lack of e x p e r i m e n t a l a t t e n t i o n is surprising in view of the fact that the h u m a n oral system is e n d o w e d with m a n y reflex p a t h w a y s c a p a b l e o f p o w e r f u l m o d u l a t i n g
Correspondence to: Dr. Anne Smith, Department of Audiology and Speech Sciences, Purdue University, West Lafayette, IN 47907 (U.S.A.).
effects o n c r a n i o f a c i a l m o t o n e u r o n pools, p a t h w a y s that are t h o u g h t to p l a y a role in swallowing, m a s t i c a t i o n , p o s t u r a l stability, a n d possibly, speech p r o d u c t i o n ( G o l d b e r g 1971; G o d a u x a n d D e s m e d t 1975; C o o k e r et al. 1980; L u n d a n d Olsson 1983; L u n d et al. 1983; S m i t h et al. 1985). I n a n earlier s t u d y f r o m this l a b o r a t o r y (Smith et al. 1985), responses of the j a w - c l o s i n g system to i n n o c u o u s m e c h a n i c a l stimuli a p p l i e d to 8 i n t r a o r a l sites were e x a m i n e d in a g r o u p of 35 y o u n g a d u l t women. Responses were m e a s u r e d as changes in j a w - c l o s i n g force a n d m a s s e t e r E M G s . T h e results i n d i c a t e d a striking s p a t i a l o r g a n i z a t i o n of reflex responses, with s o m e int r a o r a l sites p r o d u c i n g e x c i t a t o r y E M G responses a n d increases in j a w - c l o s i n g force, a n d o t h e r sites p r o d u c i n g s u p p r e s s i o n s of E M G a n d decreases in the b a c k g r o u n d b i t i n g force. In the p r e s e n t investigation, we d e s c r i b e the reflex responses p r o d u c e d in y o u n g girls a n d elderly w o m e n b y s t i m u l a t i o n of 4 of the sites s t u d i e d earlier in young adult women.
Methods
Subjects Subjects were 25 girls aged 7 a n d 8 years a n d 25 w o m e n aged 7 0 - 8 0 years. F o r c o m p a r a t i v e purposes, results f r o m an earlier s t u d y (Smith et al. 1985), using essentially the s a m e m e t h o d s of s t i m u l a t i o n a n d re-
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM
119
sponse quantification for 35 young adult women (aged 18-25 years), were available. Subjects had no history of neurological disorders, speech/language impairments, or temporomandibular joint pain. Prospective subjects were excluded if they had any condition, such as missing teeth or dental appliances, that could interfere either with maintenance of a comfortable biting force or with placement of the probe for stimulation. Procedures used in this experiment were reviewed and approved by Purdue University's Committee on the Use of Human Subjects. Informed consent was obtained from children and their parents and from the elderly subjects.
Stimulus The mechanical stimulus was created by displacement o f a servo-controlled probe mounted on a flexible arm so that it was easily positioned for stimulation of different sites. The probe was constructed of stainless steel wire that terminated in a flat, smooth, disk-shaped surface 4.5 mm in diameter. The probe excursion was a single cosine-shaped pulse of 1.0 mm amplitude and 12 msec duration (see Fig. 3). The probe was positioned so that the disk moved parallel with, rather than orthogonal to, the surface of the lingual or palatal mucosa, thereby producing a superficial, localized stimulus. Prior to onset of stimulation, the disk was placed in light contact with the mucosa.
Stimulation sites Illustrated in Fig. 1 and described below are the 4 intraoral sites selected for mechanical stimulation: AP - anterior palate, at the midline in the region of the palatal rugae. MP - midpalate, at midline, at a point one-half the length of the hard palate in the anterior-posterior dimension, in the vault of the boney palate.
AP MP
A T - anterior tongue, at midline approximately 5 mm posterior to the anterior border of the tongue tip. LT - lateral tongue, a point was located at the midline, halfway between the tip and the foramen cecum, and LT was to the right of this point, approximately 5 mm from the lateral edge of the tongue dorsum.
EMG and force recording The electrical activity of right and left masseter muscles was recorded with Ag-AgC1 disk electrodes attached to the skin overlying the muscle. Electrodes were positioned at the superior and inferior borders of the main belly of each muscle. E M G signals were amplified (20 H z - 8 kHz bandpass) and full-wave rectified. To record jaw-closing force and to stablilize the position of the mandible, a capacitive force transducer was placed in the mouth on the left side between the molars. Upper and lower bite blocks were made with dental impression material applied to the upper and lower surfaces of the transducer. After stimulation of each site, subjects could remove the force transducer, but they were instructed to re-position the transducer in their mouths so that their teeth always 'fit' the impression material. This ensured that the same position on the force transducer was maintained during the test of each site of stimulation. The intermolar separation required by the dimensions of the force transducer produced an interincisal distance of approximately 1 cm.
Experimental procedure Subjects were seated in a dental chair with an adjustable support to stabilize the position of the head. Force feedback was provided on an oscilloscope so that subjects could maintain a constant level of jaw-closing force during the application of 50 stimuli at each site. The experimental protocol was designed so that each
71
i I
LT AT
Fig. 1. Intra-oral stimulation sites; AP, anterior palate; MP, mid-palate; AT, anterior tongue; LT, lateral tongue•
120 site would be tested while subjects held 2 levels of biting force: 5 and 10 N for the children, and 10 and 20 N for the elderly. Most of the children (19 of 25), however, found the 10 N force too high to maintain steadily and comfortably; therefore in these subjects, stimulation was repeated at the 5 N level. Five of the 25 elderly subjects found the 20 N force level too high to maintain comfortably, and stimulation was repeated at the 10 N level. For each site of stimulation, the probe tip was positioned, the subject was instructed to hold the required force level, and a total of 50 stimuli were delivered. The subject rested for approximately 30 sec; then the probe was positioned to repeat stimulation of the same site or was moved to stimulate a new site. The onset of the stimulus was triggered at random intervals ranging from 700 to 1200 msec. The delivery of 50 stimuli took approximately 1 min. Throughout this period, subjects were closely monitored by an experimenter to ensure that the probe did not touch the teeth, that subjects maintained the required level of force, and that the subject did not move. The probe position in the mouth was viewed with a dental mirror, and subjects were instructed to signal the experimenter if they could not feel the mechanical stimulus. In cases in which the probe lost contact or hit the teeth, the series of stimuli was terminated; the probe was repositioned, and stimulation began again. The rectified EMG, force, and stimulus probe position signals were recorded on FM tape (DC to 1250 Hz bandpass) for subsequent analysis. Control condition At the beginning of each experimental session, a control condition was completed. The probe was placed approximately 2 cm from the lips, and 50 stimuli were delivered. This condition allowed assessment of possible responses produced by the weak auditory stimulus generated by the movement of the servo-controlled probe. Measurement of responses Responses were measured from averaged records of force and rectified EMG. A computer was used to obtain the average response to 50 stimuli. A pulse occurring 32 msec before the onset of the mechanical stimulus was used to trigger the averaging program. A 500 msec period was averaged; the sampling rate was 2000 samples/sec for jaw-closing force and stimulus position and 5000 samples/sec for the EMGs. Averaged force and E M G records were displayed on a computer terminal. The peak-to-peak change in jawclosing force in the 200 msec interval following the stimulus was calculated. In addition, the direction of any obvious changes in force from the baseline level was noted (increase or decrease). The E M G records from the right and left masseter muscles were judged as either containing a response, an
A. SMITH ET AL. obvious change from the baseline E M G activity, or no response. If a response was judged to be present, the pattern of the response was noted. Responses were classified according to type (suppression or excitation) and number of components present. The latency of the onset of E M G responses was measured with the aid of the simultaneous display of the cumulative sum for each E M G average (Ellaway 1978). The onset was selected as the first point where the averaged E M G deviated from the prestimulus baseline. The amplitude of the first component of E M G responses was measured by calculating the definite integral of the voltage over the duration of the first component and expressing this value as a percent change from an integral calculated over an identical period of time in the prestimulus interval (Smith et al. 1987). In a few cases in which the duration of the first component of the E M G response was longer than the prestimulus interval of 32 msec, the amplitude was calculated only from the first 32 msec of the E M G response.
Results Control condition In this condition, subjects maintained either a 5 N (children) or 10 N (elderly) biting force while stimulation occurred without the probe in contact. Peak-to-peak force changes ranged from 0.04 to 0.18 N; means were 0.11 N (S.D., 0.08) for the children and 0.08 N (S.D., 0.03) for the elderly. No E M G responses were observed in this condition. Thus, the weak auditory stimulus created by the movement of the probe did not elicit measurable reflex responses, and the peak-to-peak changes observed in the averaged jaw-closing force were interpreted as a measure of each subject's background instability in maintaining the target force. Because there was a high degree of intersubject variability on this measure, particularly in the children, the peak-to-peak change in force observed in the control condition for each subject was used to aid in classification of force responses to intraoral stimulation. To be classified as a response, the peak-to-peak force change observed for an individual to tactile stimulation had to meet 2 criteria: (1) its amplitude had to exceed the amplitude of the force change observed for that individual in the control condition, and (2) the onset of the force change had to occur after stimulation. If a force record did not meet these criteria, it was classified as no response. Force responses The numbers of force records classified as response and no response for the two groups for each site of stimulation are shown in Table I. The number of possible observations or records for each group at each site is 50 (25 subjects × 2 averages/subject). Less than 50 were
REFLEXES OF THE H U M A N JAW-CLOSING SYSTEM
121
TABLE I Percentage of average force records classified as response (R) and no response (NR). Site
Child
Elderly
No. of records
R (%)
NR (%)
50 49 48 49
82 82 75 86
18 18 25 14
196
81
19
AP MP AT LT All sites
No. of records
X2 R (%)
NR (%)
50 49 50 50
72 59 76 72
28 41 24 28
199
70
30
2.8 12.6 * * 0.03 4.7 *
* P < 0.05. * * P < 0.001.
sometimes available for analysis, because a few (4 of 200 for the children and I of 200 for the elderly) records were lost or discarded due to technical problems. Chisquare statistics were calculated for each site to test for differences in proportions of responses and no responses between the two groups. Values of the chi-square are listed in Table I. For MP and LT, the elderly had significantly fewer force responses. Table II summarizes the direction of the initial changes from the background biting force in those records classified as showing a force response and includes the mean peak-to-peak force change in the first 200 msec following stimulation. Within each group, data for the two background biting forces have been combined. It should be noted that force responses were often complex with periods of both increased and decreased force relative to the background biting force. Table II only indicates the direction of the initial component of the force response. For the children, the initial direction of force change with stimulation of the palate is predominantly a drop in force, while stimulation of the tongue primarily produces increases in the background biting force. For the elderly, the predominant initial force response is a decrease with stimulation of AP, MP and AT, but with stimulation of LT, the most frequent response is an increase. Table II indicates the mean peak-to-peak changes in jaw-closing force were higher for the children than for
elderly for 3 of the 4 stimulation sites. These measures are difficult to interpret, however, due to the fact that the children and elderly did not maintain the same background biting forces. In Table III, the mean peakto-peak changes in force following stimulation are expressed as a percentage change from the background biting force, and values of the Student's t statistic calculated for differences between groups for each site are reported. Force responses of the children, expressed as a percent change from background biting force, are significantly larger for all sites of stimulation. E M G responses
Table IV summarizes the numbers of E M G records classified as showing a response or no response to stimulation. Data from the right and left masseter recordings are combined, so that for each group and each stimulation site, the total number of possible observations is 100 (25 subjects x 2 repetitions of stimulation at each site/subject x 2 E M G recordings/subject). Chisquare statistics were used to test for differences between the two groups in occurrence of the response and no response categories. Values of the chi-square are shown in the last column of Table IV. For all sites, the elderly had significantly reduced numbers of responses in the E M G records. The graphs in Fig. 2 show the sign and latency of the first component of all of the E M G responses for the
TABLE II Direction of the initial changes in force responses (expressed as a percentage of the total number of responses at that site) and mean peak-to-peak amplitude (in newtons) of responses. Site
AP MP AT LT
Child
Elderly
No. of responses
Increase (%)
Decrease (%)
Mean amp.
No. of responses
Increase (%)
Decrease (%)
Mean amp.
41 40 36 42
10 33 86 88
90 67 14 12
0.43 0.38 0.33 0.43
36 29 38 36
22 41 34 67
78 59 66 33
0.30 0.38 0.29 0.28
A. S M I T H E T AL.
122 T A B L E III The m e a n s a n d s t a n d a r d d e v i a t i o n s of the p e a k - t o - p e a k c h a n g e s in force expressed as a p e r c e n t a g e of the b a c k g r o u n d b i t i n g forces. Stimulation site AP MP AT LT
Children
Elderly
Student's t
7.5 7.4 6.7 5.6 6.1 7.5 7.5 10.0
2.3 1.9 2.7 1.9 2.2 1.7 2.1 1.9
4.0 * *
Mean S.D. Mean S.D. Mean S.D. Mean S.D.
3.6 * * 3.2 * 3.2 *
* P < 0.01. * * P < 0.001.
two groups. The sign of the response is indicated by ' + , ' an excitation, or ' - , ' a suppression of the background E M G activity. These symbols are plotted above ( + ) or below ( - ) a horizontal line representing the background E M G activity. Latency of the onset of a response is indicated by the position of the symbol along the horizontal axis on which time is marked in 5 msec intervals. To interpret the plots, it should be noted that there is no representation of the amplitude or duration of the responses. The number of symbols at a particular time represents the frequency with which a response with that latency was observed. Fig. 2 reinforces the finding summarized in Table IV that the elderly had fewer E M G responses than the children. In addition, Fig. 2 demonstrates that the nature of the first component of the E M G responses of the children varied with different stimulation sites. In contrast, the first components of the E M G responses of the elderly are similar for the AP, MP, and AT sites, that is, either a short-latency suppression or a longer latency excitation is observed. Only lateral tongue stimulation produced short-latency excitations in the elderly.
The only stimulation site off-midline was LT. The E M G summary of Fig. 2 indicates that stimulation of this site resulted in a strongly lateralized response in the children, with a preponderance of excitatory responses on the stimulated (right) side. Fig. 3 illustrates the lateralized response to stimulation of LT for one child. In the elderly, stimulation of LT produced a few excitatory E M G responses, and these also showed a tendency for lateralization, that is, the short-latency excitation occurs more frequently in E M G responses recorded from the right side. Measurement of the amplitude of the first component of the E M G responses revealed that, for responses in which the first component was a suppression of ongoing E M G activity, the amplitude of the first component tended to be similar for the children and the elderly. For example, in response to AP stimulation, an initial suppression of activity was characteristic of both groups. For the elderly the mean amplitude of the initial suppressions with AP stimulation was 36% (expressed as a percent change from the baseline EMG); and for the children, the mean amplitude was - 3 4 % . When excitatory responses were observed, however, the amplitude of the responses tended to be much larger in the children. For example, the right masseter initial excitatory response to stimulation of LT had a mean of +151% in the children. For the elderly who showed this excitatory response, the mean amplitude was + 72%. E M G responses also were classified as being simple or complex. Simple responses contained only one component, while complex responses were those in which an initial excitation or suppression was followed by one or more additional component(s). No difference was found in the two groups in the numbers of simple and complex responses. Stimulation of the lateral tongue resuited in the largest percentages of simple responses; for children 47% of responses to LT stimulation were simple and for the elderly 54% were simple. For AP, MP, and AT stimulation the majority of responses were complex. Taking all of the sites together, two-thirds of all responses were complex (children, 66%, and elderly, 67%). -
T A B L E IV Percentages of E M G records classified as responses (R) a n d no r e s p o n s e s (NR). D a t a from right a n d left m a s s e t e r recordings have been c o m b i n e d . Site
Child
Elderly
X2
No. of records
R (%)
NR (%)
No. of records
R (%)
NR (%)
AP MP AT LT
100 98 96 98
80 74 80 81
20 26 20 19
100 98 100 100
62 44 58 38
38 56 42 62
All sites
392
79
21
398
51
49
* P < 0.01. * * P < 0.001.
7.9 18.6 11.3 38.4
* ** ** **
REFLEXES OF THE H U M A N JAW-CLOSING SYSTEM
123
Comparison of young adult (YA) responses with those of the elderly (E) and children (C) Force responses. The percentages of force records
the 4 stimulation sites. The Y A group had the largest percentage of force responses. The difference between the Y A and E groups was significant (X 2 = 12.5, P < 0.001), but C-YA (X 2 = 3.3) and C-E (X 2 = 3.3) comparisons were not significant. The means, standard deviations, and ranges of peakto-peak amplitudes of force responses for each group
categorized as response (R) and no response (NR) were R = 81%, N R = 19% for the children, R = 90%, N R = 10% for the young adults, and R = 70%, N R = 30% for the elderly. Percentages represent results combined for
RIGHT MASSETER EMG RESPONSE Latency
LEFT MASSETER EMG RESPONSE Latency (ms)
(ms)
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Fig. 2. Frequency of occurrence of initial excitatory components ( + ) and initial suppressions of activity ( - ) in the EMG responses to stimulation at each of the 4 sites. Children's responses: top 4 panels. Elderly responses: bottom 4 panels. The position of each + or - along the horizontal axis indicates the latency of the response in msec. The number of responses at each latency is indicated on the vertical axis. Close inspection of this figure suggests that there may be an unexpected asymmetry in the latency of responses of the children to stimulation of the anterior palate site. For the children, the responses in left masseter were in fact significantly shorter in latency than those on the right side. The mean latency of the right and left responses was 19.5 and 17.0 msec respectively (paired t = 3.7, P < 0.001). Right and left EMG responses of the elderly were not significantly different.
124
A. SMITH ET AL.
LT
TABLE VI Percentages of short-latency ( < 25 msec) E M G responses showing an excitation (EX) or suppression (S) for the children (C), young adults (YA), and elderly (E). Stimulation site MP AT
EX S EX S
C (%)
YA (%)
E (%)
39 61 54 46
9 91 30 70
0 100 4 96
lmmL-- ~ i
400
ms
q
Fig. 3. The averaged response of one child to stimulation of the lateral tongue site. The top two traces are the right (first trace) and left masseter (second trace) EMGs. The horizontal line under the EMGs represents zero activation. The third trace is jaw-closing force. The bottom trace shows the position of the stimulus probe.
are given in Table V. The last column of Table V expresses each mean as a percentage of the background biting force. Data are combined for the 4 stimulation sites, but include data from only one force feedback level, 5 N for the children and 10 N for both of the adult groups. A Student's t statistic computed for the force responses in newtons of the YA and E groups indicated the YA mean was significantly higher (t = 2.8, P < 0.01). To compare C and YA groups, a t statistic was computed on the force changes expressed as a percentage change from baseline, because of the differences in background biting force. This test revealed that the children had significantly larger force responses relative to background (t = 5.38, P < 0.001). Statistical tests for differences in the amplitudes of force responses of the children and elderly have already been reported (Table III). E M G responses. The percentages of E M G records classified as response and no response for the 3 groups were R = 79%, N R = 21% for the children, R = 68%, N R = 32% for the young adults, and R = 51%, N R = 49% for the elderly. Data from all stimulation sites were combined. Children had the highest number of observable E M G responses, and the elderly had the fewest.
TABLE V Mean peak-to-peak amplitude, standard deviation and range (in newtons) of force responses of the children (C), young adults (YA) and elderly (E). The last column shows the mean expressed as a percentage change from the background biting force.
C YA E
Mean (N)
S.D. (N)
Range (N)
Mean % change
0.41 0.38 0.29
0.42 0.23 0.20
0.06-2.70 0.10-1.70 0.06-0.95
8.2 3.8 2.9
Chi-square statistics for group differences in proportions of r e s p o n s e / n o response categories were: C-YA, X 2 = 3 . 1 , P < 0 . 1 ; C-E, X 2=17.2, P < 0 . 0 0 1 ; YA-E, X 2 = 6.0, P < 0.02. Only the C-YA contrast was not significant. The sign of the first component of the reflex responses in the E M G , whether an excitation or a suppression, was the same among the 3 groups for some sites of stimulation, but different for other sites. AP stimulation produced a highly consistent short-latency (arbitrarily defined as < 25 msec, see Smith et al. 1985) suppression of masseter activity in all 3 groups. Of the 85 subjects tested, only one, a child, showed a shortlatency excitation with stimulation of AP. Stimulation of MP, in contrast, produced different results in the 3 groups. In Table VI, the percentages of E M G responses with an initial component that was a short-latency excitation or suppression are given. As the age of the group increases, the number of short-latency excitations decreases to zero. A similar trend was observed for the A T site, and the relevant percentages are also listed in Table VI. With LT stimulation, the patterns of E M G responses were similar across the 3 groups. A shortlatency excitation in the right masseter activity was the most c o m m o n response, but the numbers of these responses in the elderly were greatly reduced compared to the young adults or children. Latencies to the onset of E M G responses for the 3 groups could be compared for the AP stimulation site, the only site for which the first component of the response was consistent both within and across groups. Mean latencies with AP stimulation were: C, 18.0 msec (S.D. = 5.6); YA, 16.2 msec (S.D. = 2.2); E, 19.4 msec (S.D. = 3.6). Student's t tests indicated that means were significantly different for C-YA (t = 3.2, P < 0.001) and for the YA-E contrast (t = 7.11, P < 0.001). The C-E comparison was not significant t (t = 1.6, P < 0.1). As indicated in Methods, patterns of E M G responses were coded by numbers of components present and the direction of each component. Children had patterns of modulation of the E M G in response to stimulation that were rarely or never observed in the elderly or young adults. In addition, there were differences in the YA and E groups in the response types that appeared most
125
REFLEXES OF T H E H U M A N J A W - C L O S I N G SYSTEM
frequently. In Fig. 4, the records labeled C-1 show an example of a short-latency excitation response of one of the children to mid-palate stimulation. This response category was defined as a short-latency excitation that could be simple (single-component response) or followed by a suppression of activity. With MP stimulation, this pattern was observed in 33% of E M G records of children, in 6% of the young adults' E M G records, and in none of the elderly EMGs. The second set of records, labeled C-2 in Fig. 4, shows a response pattern that was defined as a double suppression; it was found in 22% of children's E M G responses, 35% of YA responses, and 5% of E responses. The bottom panel of Fig. 4, labeled E, is from one elderly subject and illustrates the E M G response pattern most frequently observed (56% of responses) with MP stimulation in the elderly. This pattern (a single suppression that could be a simple response or followed by an excitation) occurred in 29% of the children's E M G responses and in 30% of the young adults' responses. Other sites of stimulation revealed similar results.
AP
C-2
5 vl_ 10 pV[
C-3
5pV]
MP IOpV L
5.vL
v
.
.
.
400 ms
.
,
Fig. 5. Averaged responses to stimulation of anterior palate for 3 children (C-1, C-2, C-3) and ! elderly subject (E). For each subject right and left masseter EMGs are shown. For each EMG trace the horizontal portion of the calibration bar indicates zero activation level. The bottom trace shows the position of the stimulus probe.
zwL zpvL
E
2o.v/ 4 pv[
j
400 ms
t
Fig. 4. Averaged responses to stimulation of midpalate for 2 children (C-1 and C-2) and 1 elderly subject (E). For each subject right and left masseter E M G s are shown. For each E M G trace the horizontal portion of the calibration bar indicates zero activation level. The bottom trace shows the position of the stimulus probe.
The summary of initial direction of E M G responses described above (Fig. 2) and in Fig. 2 of Smith et al. (1985) suggests that AP stimulation produced shortlatency suppression of masseter activity in all 3 groups. While the first components had the same direction, the duration of the first component and the nature of later components of E M G responses to AP stimulation differed among the groups. Fig. 5 shows the E M G responses of 3 children and 1 elderly subject to stimulation of the anterior palate. The two upper panels of Fig. 5, labeled C-1 and C-2, show the E M G responses from 2 children. There is a long initial suppression of activity followed by a long excitation. This pattern of E M G response was characterized by a long-lasting (greater than 40 msec), short-latency (less than 25 msec) suppression and was observed in 23% of the E M G responses of the children and in none of the E M G s of the
126
young adults or elderly. In the data of C-2, there is a suggestion of an excitatory component interrupting the long suppression of activity. As illustrated in the data of a third child, C-3 of Fig. 5, this excitatory component was fully developed in the responses of other children. This EMG response pattern was defined as a double suppression and was found in 39% of the children's E M G responses, 31% of YA responses, and only 5% of the E responses. Finally, the panel labeled E in Fig. 5 shows responses of right and left masseter in an elderly subject to stimulation of anterior palate. In this response, the second suppression has disappeared. This pattern (a single suppression that could be simple or followed by an excitation) was observed in 35% of the children's EMG responses, 68% of the YA responses, and in 79% of the E M G responses of the elderly. Discussion The results of the present investigation indicate that responses of the jaw-closing system to innocuous mechanical stimulation of the tongue and palate in groups of normal human subjects change as a function of age. Compared to the younger groups, the elderly displayed reduced responsiveness to stimulation, a change in the sign of the predominant response to stimulation of certain sites, and increased latency to onset of E M G responses. Overall responsiveness to stimulation Evidence of reduced responsiveness to stimulation with increased age is derived from both the force and EMG data. When data from the 4 sites were combined (Table V), the mean of the young adults' force responses was higher than that of the elderly. Comparison of the childrens' force responses with those of other groups is complicated by the fact that the children and adults did not hold the same background biting forces. Most of the children, probably due to the smaller size of the oral structures, could not comfortably maintain a 10 N biting force, and stimulation was repeated with a 5 N bite. Although it seems a reasonable assumption that the maximum force output of the jaw-closing system in the children would be less than that of the adults, we did not measure maximum biting force and thus have no way of assessing whether the 5 N bite of the children was in some sense 'equal' to the 10 N bite of the adults. We do know that, in the young adult group, the absolute amplitude of force responses increases when biting force is increased from 10 to 20 N (Smith et al. 1985). Therefore, it seems inappropriate to compare the absolute amplitudes of force responses of the children and adults, and peak-to-peak measures of force change were expressed as a percent change from the background biting force. Even this attempt to normalize the
A. SMITH ET AL.
data for comparisons is not optimal. From the young adult data, we also know that, when expressed as a force change relative to the baseline, the percentage change decreases as biting force increases. Expressed as a percentage change from baseline, force responses of the young adult group for the 4 stimulation sites decreased from 3.8% with a 10 N biting force, to 2.7% with a 20 N background biting force (Smith et al. 1985). Given these points, our report that percentage change from background force in the children was significantly higher than for young adults or the elderly must be interpreted with some caution. When the force data were assessed in a binary way, response vs. no response, only the YA-E comparison showed a significant reduction of responses in the elderly. Although the children did have significantly more force responses than the elderly for two stimulation sites (Table I), when percentages combined for the 4 sites were compared, the children were not significantly different from the YA or E groups. The lack of significant differences between children and the other groups on percentages of records showing a force response may be related to the fact that the childrens' force records were characterized by large background instability. Mean peak-to-peak force fluctuations observed without tactile stimulation (control condition), expressed as percentages of the background biting force, were 2.2% for the children, and 0.7% and 0.8% for the young adults and elderly, respectively. To be judged a response, peak-to-peak force changes following tactile stimulation had to exceed the value observed for that subject without tactile stimulation (control condition). Therefore, on average, force changes observed in the children had to be larger than those of the other two groups to be judged a response to stimulation. Although this was a necessary strategy to adopt, so that random fluctuations would not be included as responses, it most likely resulted in our underestimating the true number of stimulus-related force changes in the children. A clear indication of reduced responsiveness in the elderly emerged with analysis of the numbers of E M G responses present in the 3 groups. Children and the young adult group did not differ, while the elderly had a significantly lower percentage of E M G responses compared to the children and to the young adults. In fact, approximately one-half of the E M G records of the elderly were judged to contain no response. Only 30% of the force records of the elderly were classified as containing no response. This apparent discrepancy between force and E M G is explained by the fact that the force record represents the summed output of all of the jaw-closing muscles. A force response in the absence of a response in masseter recordings may arise from reflex modulation of the activity of medial pterygoid or temporalis muscles.
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM
Sign and latency of EMG responses In the group of young adult women studied earlier (Smith et al. 1985), the sign of the first component of the EMG response of masseter muscles to intra-oral stimulation was found to be dependent on the site of stimulation. Stimulation of the tongue typically produced E M G responses with initial excitatory components, while stimulation of sites on the palate produced suppressions of ongoing E M G activity. Smith et al. (1985) presented arguments that suggest that the excitatory responses are mediated by low threshold intra-oral mechanoreceptors, rather than arising from excitation of spindles in jaw-closing muscles. A number of investigators who have studied the response of the jaw closing system to electrical and mechanical stimulation of the peri-oral and intra-oral tissues refer to this set of reflexes as 'exteroceptive suppressions' (e.g., Godaux and Desmedt 1975; Cruccu et al. 1989). Given the findings from this laboratory and others (e.g., Goldberg 1971; Carels and Van Steenberghe 1986) that intra-oral mechanical stimulation can produce relatively short-latency excitation of jaw-closing muscles, this terminology should perhaps be revised. We would suggest the responses of jaw-closing muscles to intra- and peri-oral stimulation should be referred to simply as 'exteroceptive responses.' In addition to dependence on the site of stimulation, the sign of the initial component of exteroceptive responses of jaw-closing muscles also appears to be dependent on the age of the subjects. In children, shortlatency excitatory responses were common with midpalate and anterior tongue stimulation (Table VI). The percentage of E M G responses with a short-latency excitatory component decreases with stimulation of these two sites in the young adult group. By age 70, shortlatency excitatory components are rarely observed, even with lateral tongue stimulation, which, in the young adults and children, produces a highly consistent, lateralized, short-latency, excitatory response. The processes underlying this loss of short-latency excitation with age are unknown. Possible mechanisms might include a reduction in the number of a certain type of intra-oral mechanoreceptor that gives rise to the excitatory component, and changes in corticobulbar influences that, over the life span, increasingly suppress the neural connections that mediate the early excitatory response. The latency of spinal reflex responses has been considered an important index of neuromuscular changes associated with development and aging (e.g., Clarkson 1978; Issler and Stephens 1983). In the present study, reflex latencies were compared across the 3 groups for AP stimulation only. It is difficult to compare the latency of E M G responses for other sites due to differences in the sign of the initial components. Responses initiated by excitatory components tended to
127 occur earlier than those in which the initial response was a suppression (Fig. 2). Because the numbers of subjects showing the early excitatory components differed systematically with age, latency comparisons would be confounded with differences in the sign of the responses. For stimulation of the anterior palate, the sign of the initial component of the E M G response was consistent within and between groups, and the elderly had significantly longer response latencies compared to the YA group. The children had longer latencies than the young adults, but did not differ from the elderly. That children in this age group have longer latencies than young adults is not consistent with results reported for spinal cutaneous reflexes (Issler and Stephens 1983), but in rats, cats and rabbits, the latency of digastric reflex responses to intra- and peri-oral stimulation shortened with maturation (Thexton and McGarrick 1984). It seems likely that the reduced latency in the young adults compared to the children observed in the present report results from decreasing central delays. The longer latency of the elderly subjects' responses could be due to a number of factors, such as decreased size and numbers of receptors, increased peripheral conduction time, and increased central delays (Sabbahi and Sedgwick 1982; Matsuoka et al. 1983; Mathewson and Nava 1985).
Conclusion The heterogeneity of the EMG responses of the children and the presence of responses rarely or never seen in adults (Figs. 4 and 5) suggest that age 7-8 years is a transitional period in the development of oral motor reflexes. Some 7-8-year-old children have adult-like responses, while others have responses that appear to represent earlier forms or transitional responses. Investigators of cutaneous and stretch reflexes .of the limbs have found that adult-like responses begin to emerge from 6 to 8 years after birth and are generally well established by age 12 (Bawa 1981; Issler and Stephens 1983; Rowlandson and Stephens 1985). This developmental schedule is also suggested by the results of Carels and Van Steenberghe (1986), who reported that complex patterns of masseteric EMG responses to tooth stimulation were not different for children aged 10-14 years and adults. The continuing development of oral motor reflexes until age 7-8 years has important implications for our understanding of the acquisition of complex motor skills, such as those required for speech production. The results of the present study argue against the view that reflexes are present at birth as a set of 'hard-wired,' fixed, fundamental units, that must be either suppressed or marshalled into service by developing cortical motor control systems. In a discussion of similar developmental trends in spinal reflexes, Rowlandson and Stephens (1985) stated, ' . . . reflex development is the companion
128 a n d n o t the h a r b i n g e r o f d e v e l o p i n g m o t o r skills' (p. 431). Similarly, t h e p r e s e n t results s u g g e s t t h a t o r a l - m o tor reflex d e v e l o p m e n t o c c u r s in c o n c e r t w i t h d e v e l o p i n g s p e e c h m o t o r skills. S y s t e m a t i c c h a n g e s in r e f l e x r e s p o n s e s also o c c u r in t h e p e r i o d f r o m y o u n g a d u l t h o o d to the s e v e n t h d e c a d e of life. T h i s result i n d i c a t e s a continuous evolution of oral sensorimotor systems t h r o u g h o u t t h e h u m a n life span. F i n a l l y , it s h o u l d b e n o t e d that, in t h e p r e s e n t invest i g a t i o n a n d in a c o m p a n i o n p a p e r ( S m i t h et al. 1985), d u e to e v i d e n c e o f sex d i f f e r e n c e s in o r a l s e n s o r y c a p a bilities (e.g., E s s i c k et al. 1988), we c h o s e to s t u d y f e m a l e s only. It s e e m s likely, h o w e v e r , t h a t a n essentially s i m i l a r p a t t e r n of a g e - r e l a t e d c h a n g e s w o u l d c h a r a c t e r i z e o r a l - m o t o r r e f l e x e s in m a l e s . This work was supported by Grants NS19173 and CD00559 from the National Institutes of Health.
References Bawa, P. Neural development in children: a neurophysiological study. Electroenceph. clin. Neurophysiol., 1981, 52: 249-256. Berkinblit, M.B., Feldman, A.G. and Fukson, O.I. Adaptability of innate motor patterns and motor control mechanisms. Behav. Brain Sci., 1986, 9: 585-638. Cards, C. and Van Steenberghe, D. The influence of jaw position and antagonistic tooth relations on the appearance of a short-latency excitatory reflex in the human masseter muscles following mechanical tooth stimulation. Arch. Oral Biol., 1986, 31: 769-774. Clarkson, P.M. The relationship of age and level of physical activity with fractioned components of patellar reflex time. J. Gerontol., 1978, 33: 650-656. Cooker, H., Larson, C. and Luschei, E.S. Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J. Physiol. (Lond.), 1980, 308: 61-78. Cruccu, G., Agostino, R., Inghilleri, M., Manfredi, M. and Ongerboer de-Visser, B.W. The masseter inhibitory reflex is evoked by innocuous stimuli and mediated by A beta afferent fibres. Exp. Brain Res., 1989, 77: 447-450.
A. SMITH ET AL. Ellaway, P. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroenceph. clin. Neurophysiol., 1978, 45: 302-304. Essick, G.K., Afferica, T., Aldershof, B., Nestor, J., Kelly, D. and Whitsel, B. Human perioral directional sensitivity. Exp. Neurol., 1988, 100: 506-523. Godaux, E. and Desmedt, J.E. Exteroceptive suppression and motor control of the masseter and temporalis muscles in normal man. Brain Res., 1975, 85: 447-458. Goldberg, L.J. Masseter muscle excitation induced by stimulation of periodontal and gingival receptors in man. Brain Res., 1971, 32: 369-381. Hart, B.A. Fractioned myotactic reflex times in women by activity level and age. J. Gerontol., 1986, 41: 361-367. Issler, H. and Stephens, J.A. The maturation of cutaneous reflexes studied in the upper limb in man. J. Physiol. (London), 1983, 335: 643-654. Lund, J.P. and Olsson, K.A. The importance of reflexes and their control during jaw movement. Trends Neurosci., 1983, 6: 95-98. Lund, J.P., Lamarre, Y., Lavigne, G. and Duquet, G. Human jaw reflexes. In: J.E. Desmedt (Ed.), Motor Control Mechanisms in Health and Disease. Raven Press, New York, 1983: 739-755. Mathewson, R.C. and Nava, P.B. Effects of age on Meissner corpuscles: a study of silver-impregnated neurites in mouse digital pads. J. Comp. Neurol., 1985, 231: 250-259. Matsuoka, S., Suzuki, H., Morioka, S., Ogawa, Y. and Kojima, T. Quantitative and qualitative studies of Meissner's corpuscles in human skin, with special reference to alterations caused by aging. J. Dermatol., 1983, 10: 205-216. Paulson, G. and Gottlieb, G. Developmental reflexes: the reappearance of foetal and neonatal reflexes in aged patients. Brain, 1968, 91: 37-52. Rowlandson, P.H. and Stephens, J.A. Maturation of cutaneous reflex responses recorded in the lower limbs in man. Dev. Med. Child Neurol., 1985, 27: 425-433. Sabbahi, M.A. and Sedgwick, E.M. Age-related changes in monosynaptic reflex excitability. J. Gerontol., 1982, 37: 24-32. Smith, A., Moore, C.A., Weber, C.M., McFarland, D.H. and Moon, J.B. Reflex responses of the human jaw-closing system depend on the locus of intra-oral mechanical stimulation. Exp. Neurol., 1985, 90: 489-509. Smith, A., McFarland, D.H., Weber, C.M. and Moore, C.A. Spatial organization of perioral reflexes. Exp. Neurol., 1987, 98: 233-248. Thexton, A.J. and McGarrick, J.D. Maturation of brainstem reflex mechanisms in relation to the transition from liquid to solid food ingestion. Brain Behav. Evol., 1984, 25: 138-145.
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ELMOCO 89214
Developmental and age-related changes in reflexes of the human jaw-closing system Anne Smith, Christine M. Weber, Joann Newton and Margaret Denny Department of Audiology and Speech Sciences, Purdue University, West Lafayette, IN 47907 (U.S.A.)
(Accepted for publication: 25 June 1990)
Summary Reflex responses of the jaw-closing system to innocuous mechanical stimulation of the tongue and palate were examined in a group of 25 girls aged 7-8 years and in a group of 25 women aged 70-80 years. Responses were measured both as changes in background biting force and from bilateral recordings of masseter EMGs. For comparative purposes, results from an earlier study of 35 young adult women (aged 18-25 years) were available. Compared to younger groups of subjects, reflex responses of the elderly were reduced in numbers and amplitude, were characterized by fewer initial excitatory component responses, and had longer latency to onset. Analyses of responses of the children indicated that age 7-8 years is a transitional period. Some children show adult-like responses, while others display responses that appear to represent earlier forms or transitional responses. These results suggest that oral-motor reflexes are not fixed response patterns upon which more complex motor skills, such as speech, are built. Rather, oral reflex development appears to occur in concert with the acquisition of complex motor skills. Systematic changes in reflex responses also occur in the period from young adulthood to the seventh decade of life. This result indicates a continuous evolution of oral sensorimotor systems throughout the human life span. Key words: Jaw-closing system; Oral sensorimotor system; Reflex response; Mechanical stimulation; Developmental change; Age-related change
G r o w i n g awareness of the p o t e n t i a l significance of changes in reflex f u n c t i o n that m a y occur with d e v e l o p m e n t a n d aging has m o t i v a t e d n u m e r o u s investigations of stretch a n d c u t a n e o u s reflexes of the u p p e r a n d lower l i m b s in c h i l d r e n a n d elderly subjects (e.g., C l a r k s o n 1978; Bawa 1981; Issler a n d Stephens 1983; R o w l a n d son a n d Stephens 1985; H a r t 1986). T h e results of these investigations have significant i m p l i c a t i o n s for u n d e r s t a n d i n g d e v e l o p i n g m o t o r skills a n d m o t o r perform a n c e in the elderly. F u r t h e r m o r e , careful d e s c r i p t i o n s of h u m a n reflex f u n c t i o n are i m p o r t a n t clinically a n d to theories of m o t o r control, which often i n c o r p o r a t e the i d e a that m o r e c o m p l e x m o t o r b e h a v i o r s are b u i l t on a f o u n d a t i o n of pre-existing reflex circuitry (e.g., Berkinb l i t et al. 1986). I n c o n t r a s t to reflexes o f the limbs, p o s s i b l e changes in reflexes of the h u m a n o r a l - m o t o r system over the life s p a n have received little q u a n t i t a t i v e e x p e r i m e n t a l attention, a l t h o u g h the r e - e m e r g e n c e of ' p r i m i t i v e ' or ' d e v e l o p m e n t a l ' oral reflexes in aged p a t i e n t s has often b e e n d e s c r i b e d (e.g., P a u l s o n a n d G o t t l i e b 1968). This lack of e x p e r i m e n t a l a t t e n t i o n is surprising in view of the fact that the h u m a n oral system is e n d o w e d with m a n y reflex p a t h w a y s c a p a b l e o f p o w e r f u l m o d u l a t i n g
Correspondence to: Dr. Anne Smith, Department of Audiology and Speech Sciences, Purdue University, West Lafayette, IN 47907 (U.S.A.).
effects o n c r a n i o f a c i a l m o t o n e u r o n pools, p a t h w a y s that are t h o u g h t to p l a y a role in swallowing, m a s t i c a t i o n , p o s t u r a l stability, a n d possibly, speech p r o d u c t i o n ( G o l d b e r g 1971; G o d a u x a n d D e s m e d t 1975; C o o k e r et al. 1980; L u n d a n d Olsson 1983; L u n d et al. 1983; S m i t h et al. 1985). I n a n earlier s t u d y f r o m this l a b o r a t o r y (Smith et al. 1985), responses of the j a w - c l o s i n g system to i n n o c u o u s m e c h a n i c a l stimuli a p p l i e d to 8 i n t r a o r a l sites were e x a m i n e d in a g r o u p of 35 y o u n g a d u l t women. Responses were m e a s u r e d as changes in j a w - c l o s i n g force a n d m a s s e t e r E M G s . T h e results i n d i c a t e d a striking s p a t i a l o r g a n i z a t i o n of reflex responses, with s o m e int r a o r a l sites p r o d u c i n g e x c i t a t o r y E M G responses a n d increases in j a w - c l o s i n g force, a n d o t h e r sites p r o d u c i n g s u p p r e s s i o n s of E M G a n d decreases in the b a c k g r o u n d b i t i n g force. In the p r e s e n t investigation, we d e s c r i b e the reflex responses p r o d u c e d in y o u n g girls a n d elderly w o m e n b y s t i m u l a t i o n of 4 of the sites s t u d i e d earlier in young adult women.
Methods
Subjects Subjects were 25 girls aged 7 a n d 8 years a n d 25 w o m e n aged 7 0 - 8 0 years. F o r c o m p a r a t i v e purposes, results f r o m an earlier s t u d y (Smith et al. 1985), using essentially the s a m e m e t h o d s of s t i m u l a t i o n a n d re-
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM
119
sponse quantification for 35 young adult women (aged 18-25 years), were available. Subjects had no history of neurological disorders, speech/language impairments, or temporomandibular joint pain. Prospective subjects were excluded if they had any condition, such as missing teeth or dental appliances, that could interfere either with maintenance of a comfortable biting force or with placement of the probe for stimulation. Procedures used in this experiment were reviewed and approved by Purdue University's Committee on the Use of Human Subjects. Informed consent was obtained from children and their parents and from the elderly subjects.
Stimulus The mechanical stimulus was created by displacement o f a servo-controlled probe mounted on a flexible arm so that it was easily positioned for stimulation of different sites. The probe was constructed of stainless steel wire that terminated in a flat, smooth, disk-shaped surface 4.5 mm in diameter. The probe excursion was a single cosine-shaped pulse of 1.0 mm amplitude and 12 msec duration (see Fig. 3). The probe was positioned so that the disk moved parallel with, rather than orthogonal to, the surface of the lingual or palatal mucosa, thereby producing a superficial, localized stimulus. Prior to onset of stimulation, the disk was placed in light contact with the mucosa.
Stimulation sites Illustrated in Fig. 1 and described below are the 4 intraoral sites selected for mechanical stimulation: AP - anterior palate, at the midline in the region of the palatal rugae. MP - midpalate, at midline, at a point one-half the length of the hard palate in the anterior-posterior dimension, in the vault of the boney palate.
AP MP
A T - anterior tongue, at midline approximately 5 mm posterior to the anterior border of the tongue tip. LT - lateral tongue, a point was located at the midline, halfway between the tip and the foramen cecum, and LT was to the right of this point, approximately 5 mm from the lateral edge of the tongue dorsum.
EMG and force recording The electrical activity of right and left masseter muscles was recorded with Ag-AgC1 disk electrodes attached to the skin overlying the muscle. Electrodes were positioned at the superior and inferior borders of the main belly of each muscle. E M G signals were amplified (20 H z - 8 kHz bandpass) and full-wave rectified. To record jaw-closing force and to stablilize the position of the mandible, a capacitive force transducer was placed in the mouth on the left side between the molars. Upper and lower bite blocks were made with dental impression material applied to the upper and lower surfaces of the transducer. After stimulation of each site, subjects could remove the force transducer, but they were instructed to re-position the transducer in their mouths so that their teeth always 'fit' the impression material. This ensured that the same position on the force transducer was maintained during the test of each site of stimulation. The intermolar separation required by the dimensions of the force transducer produced an interincisal distance of approximately 1 cm.
Experimental procedure Subjects were seated in a dental chair with an adjustable support to stabilize the position of the head. Force feedback was provided on an oscilloscope so that subjects could maintain a constant level of jaw-closing force during the application of 50 stimuli at each site. The experimental protocol was designed so that each
71
i I
LT AT
Fig. 1. Intra-oral stimulation sites; AP, anterior palate; MP, mid-palate; AT, anterior tongue; LT, lateral tongue•
120 site would be tested while subjects held 2 levels of biting force: 5 and 10 N for the children, and 10 and 20 N for the elderly. Most of the children (19 of 25), however, found the 10 N force too high to maintain steadily and comfortably; therefore in these subjects, stimulation was repeated at the 5 N level. Five of the 25 elderly subjects found the 20 N force level too high to maintain comfortably, and stimulation was repeated at the 10 N level. For each site of stimulation, the probe tip was positioned, the subject was instructed to hold the required force level, and a total of 50 stimuli were delivered. The subject rested for approximately 30 sec; then the probe was positioned to repeat stimulation of the same site or was moved to stimulate a new site. The onset of the stimulus was triggered at random intervals ranging from 700 to 1200 msec. The delivery of 50 stimuli took approximately 1 min. Throughout this period, subjects were closely monitored by an experimenter to ensure that the probe did not touch the teeth, that subjects maintained the required level of force, and that the subject did not move. The probe position in the mouth was viewed with a dental mirror, and subjects were instructed to signal the experimenter if they could not feel the mechanical stimulus. In cases in which the probe lost contact or hit the teeth, the series of stimuli was terminated; the probe was repositioned, and stimulation began again. The rectified EMG, force, and stimulus probe position signals were recorded on FM tape (DC to 1250 Hz bandpass) for subsequent analysis. Control condition At the beginning of each experimental session, a control condition was completed. The probe was placed approximately 2 cm from the lips, and 50 stimuli were delivered. This condition allowed assessment of possible responses produced by the weak auditory stimulus generated by the movement of the servo-controlled probe. Measurement of responses Responses were measured from averaged records of force and rectified EMG. A computer was used to obtain the average response to 50 stimuli. A pulse occurring 32 msec before the onset of the mechanical stimulus was used to trigger the averaging program. A 500 msec period was averaged; the sampling rate was 2000 samples/sec for jaw-closing force and stimulus position and 5000 samples/sec for the EMGs. Averaged force and E M G records were displayed on a computer terminal. The peak-to-peak change in jawclosing force in the 200 msec interval following the stimulus was calculated. In addition, the direction of any obvious changes in force from the baseline level was noted (increase or decrease). The E M G records from the right and left masseter muscles were judged as either containing a response, an
A. SMITH ET AL. obvious change from the baseline E M G activity, or no response. If a response was judged to be present, the pattern of the response was noted. Responses were classified according to type (suppression or excitation) and number of components present. The latency of the onset of E M G responses was measured with the aid of the simultaneous display of the cumulative sum for each E M G average (Ellaway 1978). The onset was selected as the first point where the averaged E M G deviated from the prestimulus baseline. The amplitude of the first component of E M G responses was measured by calculating the definite integral of the voltage over the duration of the first component and expressing this value as a percent change from an integral calculated over an identical period of time in the prestimulus interval (Smith et al. 1987). In a few cases in which the duration of the first component of the E M G response was longer than the prestimulus interval of 32 msec, the amplitude was calculated only from the first 32 msec of the E M G response.
Results Control condition In this condition, subjects maintained either a 5 N (children) or 10 N (elderly) biting force while stimulation occurred without the probe in contact. Peak-to-peak force changes ranged from 0.04 to 0.18 N; means were 0.11 N (S.D., 0.08) for the children and 0.08 N (S.D., 0.03) for the elderly. No E M G responses were observed in this condition. Thus, the weak auditory stimulus created by the movement of the probe did not elicit measurable reflex responses, and the peak-to-peak changes observed in the averaged jaw-closing force were interpreted as a measure of each subject's background instability in maintaining the target force. Because there was a high degree of intersubject variability on this measure, particularly in the children, the peak-to-peak change in force observed in the control condition for each subject was used to aid in classification of force responses to intraoral stimulation. To be classified as a response, the peak-to-peak force change observed for an individual to tactile stimulation had to meet 2 criteria: (1) its amplitude had to exceed the amplitude of the force change observed for that individual in the control condition, and (2) the onset of the force change had to occur after stimulation. If a force record did not meet these criteria, it was classified as no response. Force responses The numbers of force records classified as response and no response for the two groups for each site of stimulation are shown in Table I. The number of possible observations or records for each group at each site is 50 (25 subjects × 2 averages/subject). Less than 50 were
REFLEXES OF THE H U M A N JAW-CLOSING SYSTEM
121
TABLE I Percentage of average force records classified as response (R) and no response (NR). Site
Child
Elderly
No. of records
R (%)
NR (%)
50 49 48 49
82 82 75 86
18 18 25 14
196
81
19
AP MP AT LT All sites
No. of records
X2 R (%)
NR (%)
50 49 50 50
72 59 76 72
28 41 24 28
199
70
30
2.8 12.6 * * 0.03 4.7 *
* P < 0.05. * * P < 0.001.
sometimes available for analysis, because a few (4 of 200 for the children and I of 200 for the elderly) records were lost or discarded due to technical problems. Chisquare statistics were calculated for each site to test for differences in proportions of responses and no responses between the two groups. Values of the chi-square are listed in Table I. For MP and LT, the elderly had significantly fewer force responses. Table II summarizes the direction of the initial changes from the background biting force in those records classified as showing a force response and includes the mean peak-to-peak force change in the first 200 msec following stimulation. Within each group, data for the two background biting forces have been combined. It should be noted that force responses were often complex with periods of both increased and decreased force relative to the background biting force. Table II only indicates the direction of the initial component of the force response. For the children, the initial direction of force change with stimulation of the palate is predominantly a drop in force, while stimulation of the tongue primarily produces increases in the background biting force. For the elderly, the predominant initial force response is a decrease with stimulation of AP, MP and AT, but with stimulation of LT, the most frequent response is an increase. Table II indicates the mean peak-to-peak changes in jaw-closing force were higher for the children than for
elderly for 3 of the 4 stimulation sites. These measures are difficult to interpret, however, due to the fact that the children and elderly did not maintain the same background biting forces. In Table III, the mean peakto-peak changes in force following stimulation are expressed as a percentage change from the background biting force, and values of the Student's t statistic calculated for differences between groups for each site are reported. Force responses of the children, expressed as a percent change from background biting force, are significantly larger for all sites of stimulation. E M G responses
Table IV summarizes the numbers of E M G records classified as showing a response or no response to stimulation. Data from the right and left masseter recordings are combined, so that for each group and each stimulation site, the total number of possible observations is 100 (25 subjects x 2 repetitions of stimulation at each site/subject x 2 E M G recordings/subject). Chisquare statistics were used to test for differences between the two groups in occurrence of the response and no response categories. Values of the chi-square are shown in the last column of Table IV. For all sites, the elderly had significantly reduced numbers of responses in the E M G records. The graphs in Fig. 2 show the sign and latency of the first component of all of the E M G responses for the
TABLE II Direction of the initial changes in force responses (expressed as a percentage of the total number of responses at that site) and mean peak-to-peak amplitude (in newtons) of responses. Site
AP MP AT LT
Child
Elderly
No. of responses
Increase (%)
Decrease (%)
Mean amp.
No. of responses
Increase (%)
Decrease (%)
Mean amp.
41 40 36 42
10 33 86 88
90 67 14 12
0.43 0.38 0.33 0.43
36 29 38 36
22 41 34 67
78 59 66 33
0.30 0.38 0.29 0.28
A. S M I T H E T AL.
122 T A B L E III The m e a n s a n d s t a n d a r d d e v i a t i o n s of the p e a k - t o - p e a k c h a n g e s in force expressed as a p e r c e n t a g e of the b a c k g r o u n d b i t i n g forces. Stimulation site AP MP AT LT
Children
Elderly
Student's t
7.5 7.4 6.7 5.6 6.1 7.5 7.5 10.0
2.3 1.9 2.7 1.9 2.2 1.7 2.1 1.9
4.0 * *
Mean S.D. Mean S.D. Mean S.D. Mean S.D.
3.6 * * 3.2 * 3.2 *
* P < 0.01. * * P < 0.001.
two groups. The sign of the response is indicated by ' + , ' an excitation, or ' - , ' a suppression of the background E M G activity. These symbols are plotted above ( + ) or below ( - ) a horizontal line representing the background E M G activity. Latency of the onset of a response is indicated by the position of the symbol along the horizontal axis on which time is marked in 5 msec intervals. To interpret the plots, it should be noted that there is no representation of the amplitude or duration of the responses. The number of symbols at a particular time represents the frequency with which a response with that latency was observed. Fig. 2 reinforces the finding summarized in Table IV that the elderly had fewer E M G responses than the children. In addition, Fig. 2 demonstrates that the nature of the first component of the E M G responses of the children varied with different stimulation sites. In contrast, the first components of the E M G responses of the elderly are similar for the AP, MP, and AT sites, that is, either a short-latency suppression or a longer latency excitation is observed. Only lateral tongue stimulation produced short-latency excitations in the elderly.
The only stimulation site off-midline was LT. The E M G summary of Fig. 2 indicates that stimulation of this site resulted in a strongly lateralized response in the children, with a preponderance of excitatory responses on the stimulated (right) side. Fig. 3 illustrates the lateralized response to stimulation of LT for one child. In the elderly, stimulation of LT produced a few excitatory E M G responses, and these also showed a tendency for lateralization, that is, the short-latency excitation occurs more frequently in E M G responses recorded from the right side. Measurement of the amplitude of the first component of the E M G responses revealed that, for responses in which the first component was a suppression of ongoing E M G activity, the amplitude of the first component tended to be similar for the children and the elderly. For example, in response to AP stimulation, an initial suppression of activity was characteristic of both groups. For the elderly the mean amplitude of the initial suppressions with AP stimulation was 36% (expressed as a percent change from the baseline EMG); and for the children, the mean amplitude was - 3 4 % . When excitatory responses were observed, however, the amplitude of the responses tended to be much larger in the children. For example, the right masseter initial excitatory response to stimulation of LT had a mean of +151% in the children. For the elderly who showed this excitatory response, the mean amplitude was + 72%. E M G responses also were classified as being simple or complex. Simple responses contained only one component, while complex responses were those in which an initial excitation or suppression was followed by one or more additional component(s). No difference was found in the two groups in the numbers of simple and complex responses. Stimulation of the lateral tongue resuited in the largest percentages of simple responses; for children 47% of responses to LT stimulation were simple and for the elderly 54% were simple. For AP, MP, and AT stimulation the majority of responses were complex. Taking all of the sites together, two-thirds of all responses were complex (children, 66%, and elderly, 67%). -
T A B L E IV Percentages of E M G records classified as responses (R) a n d no r e s p o n s e s (NR). D a t a from right a n d left m a s s e t e r recordings have been c o m b i n e d . Site
Child
Elderly
X2
No. of records
R (%)
NR (%)
No. of records
R (%)
NR (%)
AP MP AT LT
100 98 96 98
80 74 80 81
20 26 20 19
100 98 100 100
62 44 58 38
38 56 42 62
All sites
392
79
21
398
51
49
* P < 0.01. * * P < 0.001.
7.9 18.6 11.3 38.4
* ** ** **
REFLEXES OF THE H U M A N JAW-CLOSING SYSTEM
123
Comparison of young adult (YA) responses with those of the elderly (E) and children (C) Force responses. The percentages of force records
the 4 stimulation sites. The Y A group had the largest percentage of force responses. The difference between the Y A and E groups was significant (X 2 = 12.5, P < 0.001), but C-YA (X 2 = 3.3) and C-E (X 2 = 3.3) comparisons were not significant. The means, standard deviations, and ranges of peakto-peak amplitudes of force responses for each group
categorized as response (R) and no response (NR) were R = 81%, N R = 19% for the children, R = 90%, N R = 10% for the young adults, and R = 70%, N R = 30% for the elderly. Percentages represent results combined for
RIGHT MASSETER EMG RESPONSE Latency
LEFT MASSETER EMG RESPONSE Latency (ms)
(ms)
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j
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Fig. 2. Frequency of occurrence of initial excitatory components ( + ) and initial suppressions of activity ( - ) in the EMG responses to stimulation at each of the 4 sites. Children's responses: top 4 panels. Elderly responses: bottom 4 panels. The position of each + or - along the horizontal axis indicates the latency of the response in msec. The number of responses at each latency is indicated on the vertical axis. Close inspection of this figure suggests that there may be an unexpected asymmetry in the latency of responses of the children to stimulation of the anterior palate site. For the children, the responses in left masseter were in fact significantly shorter in latency than those on the right side. The mean latency of the right and left responses was 19.5 and 17.0 msec respectively (paired t = 3.7, P < 0.001). Right and left EMG responses of the elderly were not significantly different.
124
A. SMITH ET AL.
LT
TABLE VI Percentages of short-latency ( < 25 msec) E M G responses showing an excitation (EX) or suppression (S) for the children (C), young adults (YA), and elderly (E). Stimulation site MP AT
EX S EX S
C (%)
YA (%)
E (%)
39 61 54 46
9 91 30 70
0 100 4 96
lmmL-- ~ i
400
ms
q
Fig. 3. The averaged response of one child to stimulation of the lateral tongue site. The top two traces are the right (first trace) and left masseter (second trace) EMGs. The horizontal line under the EMGs represents zero activation. The third trace is jaw-closing force. The bottom trace shows the position of the stimulus probe.
are given in Table V. The last column of Table V expresses each mean as a percentage of the background biting force. Data are combined for the 4 stimulation sites, but include data from only one force feedback level, 5 N for the children and 10 N for both of the adult groups. A Student's t statistic computed for the force responses in newtons of the YA and E groups indicated the YA mean was significantly higher (t = 2.8, P < 0.01). To compare C and YA groups, a t statistic was computed on the force changes expressed as a percentage change from baseline, because of the differences in background biting force. This test revealed that the children had significantly larger force responses relative to background (t = 5.38, P < 0.001). Statistical tests for differences in the amplitudes of force responses of the children and elderly have already been reported (Table III). E M G responses. The percentages of E M G records classified as response and no response for the 3 groups were R = 79%, N R = 21% for the children, R = 68%, N R = 32% for the young adults, and R = 51%, N R = 49% for the elderly. Data from all stimulation sites were combined. Children had the highest number of observable E M G responses, and the elderly had the fewest.
TABLE V Mean peak-to-peak amplitude, standard deviation and range (in newtons) of force responses of the children (C), young adults (YA) and elderly (E). The last column shows the mean expressed as a percentage change from the background biting force.
C YA E
Mean (N)
S.D. (N)
Range (N)
Mean % change
0.41 0.38 0.29
0.42 0.23 0.20
0.06-2.70 0.10-1.70 0.06-0.95
8.2 3.8 2.9
Chi-square statistics for group differences in proportions of r e s p o n s e / n o response categories were: C-YA, X 2 = 3 . 1 , P < 0 . 1 ; C-E, X 2=17.2, P < 0 . 0 0 1 ; YA-E, X 2 = 6.0, P < 0.02. Only the C-YA contrast was not significant. The sign of the first component of the reflex responses in the E M G , whether an excitation or a suppression, was the same among the 3 groups for some sites of stimulation, but different for other sites. AP stimulation produced a highly consistent short-latency (arbitrarily defined as < 25 msec, see Smith et al. 1985) suppression of masseter activity in all 3 groups. Of the 85 subjects tested, only one, a child, showed a shortlatency excitation with stimulation of AP. Stimulation of MP, in contrast, produced different results in the 3 groups. In Table VI, the percentages of E M G responses with an initial component that was a short-latency excitation or suppression are given. As the age of the group increases, the number of short-latency excitations decreases to zero. A similar trend was observed for the A T site, and the relevant percentages are also listed in Table VI. With LT stimulation, the patterns of E M G responses were similar across the 3 groups. A shortlatency excitation in the right masseter activity was the most c o m m o n response, but the numbers of these responses in the elderly were greatly reduced compared to the young adults or children. Latencies to the onset of E M G responses for the 3 groups could be compared for the AP stimulation site, the only site for which the first component of the response was consistent both within and across groups. Mean latencies with AP stimulation were: C, 18.0 msec (S.D. = 5.6); YA, 16.2 msec (S.D. = 2.2); E, 19.4 msec (S.D. = 3.6). Student's t tests indicated that means were significantly different for C-YA (t = 3.2, P < 0.001) and for the YA-E contrast (t = 7.11, P < 0.001). The C-E comparison was not significant t (t = 1.6, P < 0.1). As indicated in Methods, patterns of E M G responses were coded by numbers of components present and the direction of each component. Children had patterns of modulation of the E M G in response to stimulation that were rarely or never observed in the elderly or young adults. In addition, there were differences in the YA and E groups in the response types that appeared most
125
REFLEXES OF T H E H U M A N J A W - C L O S I N G SYSTEM
frequently. In Fig. 4, the records labeled C-1 show an example of a short-latency excitation response of one of the children to mid-palate stimulation. This response category was defined as a short-latency excitation that could be simple (single-component response) or followed by a suppression of activity. With MP stimulation, this pattern was observed in 33% of E M G records of children, in 6% of the young adults' E M G records, and in none of the elderly EMGs. The second set of records, labeled C-2 in Fig. 4, shows a response pattern that was defined as a double suppression; it was found in 22% of children's E M G responses, 35% of YA responses, and 5% of E responses. The bottom panel of Fig. 4, labeled E, is from one elderly subject and illustrates the E M G response pattern most frequently observed (56% of responses) with MP stimulation in the elderly. This pattern (a single suppression that could be a simple response or followed by an excitation) occurred in 29% of the children's E M G responses and in 30% of the young adults' responses. Other sites of stimulation revealed similar results.
AP
C-2
5 vl_ 10 pV[
C-3
5pV]
MP IOpV L
5.vL
v
.
.
.
400 ms
.
,
Fig. 5. Averaged responses to stimulation of anterior palate for 3 children (C-1, C-2, C-3) and ! elderly subject (E). For each subject right and left masseter EMGs are shown. For each EMG trace the horizontal portion of the calibration bar indicates zero activation level. The bottom trace shows the position of the stimulus probe.
zwL zpvL
E
2o.v/ 4 pv[
j
400 ms
t
Fig. 4. Averaged responses to stimulation of midpalate for 2 children (C-1 and C-2) and 1 elderly subject (E). For each subject right and left masseter E M G s are shown. For each E M G trace the horizontal portion of the calibration bar indicates zero activation level. The bottom trace shows the position of the stimulus probe.
The summary of initial direction of E M G responses described above (Fig. 2) and in Fig. 2 of Smith et al. (1985) suggests that AP stimulation produced shortlatency suppression of masseter activity in all 3 groups. While the first components had the same direction, the duration of the first component and the nature of later components of E M G responses to AP stimulation differed among the groups. Fig. 5 shows the E M G responses of 3 children and 1 elderly subject to stimulation of the anterior palate. The two upper panels of Fig. 5, labeled C-1 and C-2, show the E M G responses from 2 children. There is a long initial suppression of activity followed by a long excitation. This pattern of E M G response was characterized by a long-lasting (greater than 40 msec), short-latency (less than 25 msec) suppression and was observed in 23% of the E M G responses of the children and in none of the E M G s of the
126
young adults or elderly. In the data of C-2, there is a suggestion of an excitatory component interrupting the long suppression of activity. As illustrated in the data of a third child, C-3 of Fig. 5, this excitatory component was fully developed in the responses of other children. This EMG response pattern was defined as a double suppression and was found in 39% of the children's E M G responses, 31% of YA responses, and only 5% of the E responses. Finally, the panel labeled E in Fig. 5 shows responses of right and left masseter in an elderly subject to stimulation of anterior palate. In this response, the second suppression has disappeared. This pattern (a single suppression that could be simple or followed by an excitation) was observed in 35% of the children's EMG responses, 68% of the YA responses, and in 79% of the E M G responses of the elderly. Discussion The results of the present investigation indicate that responses of the jaw-closing system to innocuous mechanical stimulation of the tongue and palate in groups of normal human subjects change as a function of age. Compared to the younger groups, the elderly displayed reduced responsiveness to stimulation, a change in the sign of the predominant response to stimulation of certain sites, and increased latency to onset of E M G responses. Overall responsiveness to stimulation Evidence of reduced responsiveness to stimulation with increased age is derived from both the force and EMG data. When data from the 4 sites were combined (Table V), the mean of the young adults' force responses was higher than that of the elderly. Comparison of the childrens' force responses with those of other groups is complicated by the fact that the children and adults did not hold the same background biting forces. Most of the children, probably due to the smaller size of the oral structures, could not comfortably maintain a 10 N biting force, and stimulation was repeated with a 5 N bite. Although it seems a reasonable assumption that the maximum force output of the jaw-closing system in the children would be less than that of the adults, we did not measure maximum biting force and thus have no way of assessing whether the 5 N bite of the children was in some sense 'equal' to the 10 N bite of the adults. We do know that, in the young adult group, the absolute amplitude of force responses increases when biting force is increased from 10 to 20 N (Smith et al. 1985). Therefore, it seems inappropriate to compare the absolute amplitudes of force responses of the children and adults, and peak-to-peak measures of force change were expressed as a percent change from the background biting force. Even this attempt to normalize the
A. SMITH ET AL.
data for comparisons is not optimal. From the young adult data, we also know that, when expressed as a force change relative to the baseline, the percentage change decreases as biting force increases. Expressed as a percentage change from baseline, force responses of the young adult group for the 4 stimulation sites decreased from 3.8% with a 10 N biting force, to 2.7% with a 20 N background biting force (Smith et al. 1985). Given these points, our report that percentage change from background force in the children was significantly higher than for young adults or the elderly must be interpreted with some caution. When the force data were assessed in a binary way, response vs. no response, only the YA-E comparison showed a significant reduction of responses in the elderly. Although the children did have significantly more force responses than the elderly for two stimulation sites (Table I), when percentages combined for the 4 sites were compared, the children were not significantly different from the YA or E groups. The lack of significant differences between children and the other groups on percentages of records showing a force response may be related to the fact that the childrens' force records were characterized by large background instability. Mean peak-to-peak force fluctuations observed without tactile stimulation (control condition), expressed as percentages of the background biting force, were 2.2% for the children, and 0.7% and 0.8% for the young adults and elderly, respectively. To be judged a response, peak-to-peak force changes following tactile stimulation had to exceed the value observed for that subject without tactile stimulation (control condition). Therefore, on average, force changes observed in the children had to be larger than those of the other two groups to be judged a response to stimulation. Although this was a necessary strategy to adopt, so that random fluctuations would not be included as responses, it most likely resulted in our underestimating the true number of stimulus-related force changes in the children. A clear indication of reduced responsiveness in the elderly emerged with analysis of the numbers of E M G responses present in the 3 groups. Children and the young adult group did not differ, while the elderly had a significantly lower percentage of E M G responses compared to the children and to the young adults. In fact, approximately one-half of the E M G records of the elderly were judged to contain no response. Only 30% of the force records of the elderly were classified as containing no response. This apparent discrepancy between force and E M G is explained by the fact that the force record represents the summed output of all of the jaw-closing muscles. A force response in the absence of a response in masseter recordings may arise from reflex modulation of the activity of medial pterygoid or temporalis muscles.
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM
Sign and latency of EMG responses In the group of young adult women studied earlier (Smith et al. 1985), the sign of the first component of the EMG response of masseter muscles to intra-oral stimulation was found to be dependent on the site of stimulation. Stimulation of the tongue typically produced E M G responses with initial excitatory components, while stimulation of sites on the palate produced suppressions of ongoing E M G activity. Smith et al. (1985) presented arguments that suggest that the excitatory responses are mediated by low threshold intra-oral mechanoreceptors, rather than arising from excitation of spindles in jaw-closing muscles. A number of investigators who have studied the response of the jaw closing system to electrical and mechanical stimulation of the peri-oral and intra-oral tissues refer to this set of reflexes as 'exteroceptive suppressions' (e.g., Godaux and Desmedt 1975; Cruccu et al. 1989). Given the findings from this laboratory and others (e.g., Goldberg 1971; Carels and Van Steenberghe 1986) that intra-oral mechanical stimulation can produce relatively short-latency excitation of jaw-closing muscles, this terminology should perhaps be revised. We would suggest the responses of jaw-closing muscles to intra- and peri-oral stimulation should be referred to simply as 'exteroceptive responses.' In addition to dependence on the site of stimulation, the sign of the initial component of exteroceptive responses of jaw-closing muscles also appears to be dependent on the age of the subjects. In children, shortlatency excitatory responses were common with midpalate and anterior tongue stimulation (Table VI). The percentage of E M G responses with a short-latency excitatory component decreases with stimulation of these two sites in the young adult group. By age 70, shortlatency excitatory components are rarely observed, even with lateral tongue stimulation, which, in the young adults and children, produces a highly consistent, lateralized, short-latency, excitatory response. The processes underlying this loss of short-latency excitation with age are unknown. Possible mechanisms might include a reduction in the number of a certain type of intra-oral mechanoreceptor that gives rise to the excitatory component, and changes in corticobulbar influences that, over the life span, increasingly suppress the neural connections that mediate the early excitatory response. The latency of spinal reflex responses has been considered an important index of neuromuscular changes associated with development and aging (e.g., Clarkson 1978; Issler and Stephens 1983). In the present study, reflex latencies were compared across the 3 groups for AP stimulation only. It is difficult to compare the latency of E M G responses for other sites due to differences in the sign of the initial components. Responses initiated by excitatory components tended to
127 occur earlier than those in which the initial response was a suppression (Fig. 2). Because the numbers of subjects showing the early excitatory components differed systematically with age, latency comparisons would be confounded with differences in the sign of the responses. For stimulation of the anterior palate, the sign of the initial component of the E M G response was consistent within and between groups, and the elderly had significantly longer response latencies compared to the YA group. The children had longer latencies than the young adults, but did not differ from the elderly. That children in this age group have longer latencies than young adults is not consistent with results reported for spinal cutaneous reflexes (Issler and Stephens 1983), but in rats, cats and rabbits, the latency of digastric reflex responses to intra- and peri-oral stimulation shortened with maturation (Thexton and McGarrick 1984). It seems likely that the reduced latency in the young adults compared to the children observed in the present report results from decreasing central delays. The longer latency of the elderly subjects' responses could be due to a number of factors, such as decreased size and numbers of receptors, increased peripheral conduction time, and increased central delays (Sabbahi and Sedgwick 1982; Matsuoka et al. 1983; Mathewson and Nava 1985).
Conclusion The heterogeneity of the EMG responses of the children and the presence of responses rarely or never seen in adults (Figs. 4 and 5) suggest that age 7-8 years is a transitional period in the development of oral motor reflexes. Some 7-8-year-old children have adult-like responses, while others have responses that appear to represent earlier forms or transitional responses. Investigators of cutaneous and stretch reflexes .of the limbs have found that adult-like responses begin to emerge from 6 to 8 years after birth and are generally well established by age 12 (Bawa 1981; Issler and Stephens 1983; Rowlandson and Stephens 1985). This developmental schedule is also suggested by the results of Carels and Van Steenberghe (1986), who reported that complex patterns of masseteric EMG responses to tooth stimulation were not different for children aged 10-14 years and adults. The continuing development of oral motor reflexes until age 7-8 years has important implications for our understanding of the acquisition of complex motor skills, such as those required for speech production. The results of the present study argue against the view that reflexes are present at birth as a set of 'hard-wired,' fixed, fundamental units, that must be either suppressed or marshalled into service by developing cortical motor control systems. In a discussion of similar developmental trends in spinal reflexes, Rowlandson and Stephens (1985) stated, ' . . . reflex development is the companion
128 a n d n o t the h a r b i n g e r o f d e v e l o p i n g m o t o r skills' (p. 431). Similarly, t h e p r e s e n t results s u g g e s t t h a t o r a l - m o tor reflex d e v e l o p m e n t o c c u r s in c o n c e r t w i t h d e v e l o p i n g s p e e c h m o t o r skills. S y s t e m a t i c c h a n g e s in r e f l e x r e s p o n s e s also o c c u r in t h e p e r i o d f r o m y o u n g a d u l t h o o d to the s e v e n t h d e c a d e of life. T h i s result i n d i c a t e s a continuous evolution of oral sensorimotor systems t h r o u g h o u t t h e h u m a n life span. F i n a l l y , it s h o u l d b e n o t e d that, in t h e p r e s e n t invest i g a t i o n a n d in a c o m p a n i o n p a p e r ( S m i t h et al. 1985), d u e to e v i d e n c e o f sex d i f f e r e n c e s in o r a l s e n s o r y c a p a bilities (e.g., E s s i c k et al. 1988), we c h o s e to s t u d y f e m a l e s only. It s e e m s likely, h o w e v e r , t h a t a n essentially s i m i l a r p a t t e r n of a g e - r e l a t e d c h a n g e s w o u l d c h a r a c t e r i z e o r a l - m o t o r r e f l e x e s in m a l e s . This work was supported by Grants NS19173 and CD00559 from the National Institutes of Health.
References Bawa, P. Neural development in children: a neurophysiological study. Electroenceph. clin. Neurophysiol., 1981, 52: 249-256. Berkinblit, M.B., Feldman, A.G. and Fukson, O.I. Adaptability of innate motor patterns and motor control mechanisms. Behav. Brain Sci., 1986, 9: 585-638. Cards, C. and Van Steenberghe, D. The influence of jaw position and antagonistic tooth relations on the appearance of a short-latency excitatory reflex in the human masseter muscles following mechanical tooth stimulation. Arch. Oral Biol., 1986, 31: 769-774. Clarkson, P.M. The relationship of age and level of physical activity with fractioned components of patellar reflex time. J. Gerontol., 1978, 33: 650-656. Cooker, H., Larson, C. and Luschei, E.S. Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J. Physiol. (Lond.), 1980, 308: 61-78. Cruccu, G., Agostino, R., Inghilleri, M., Manfredi, M. and Ongerboer de-Visser, B.W. The masseter inhibitory reflex is evoked by innocuous stimuli and mediated by A beta afferent fibres. Exp. Brain Res., 1989, 77: 447-450.
A. SMITH ET AL. Ellaway, P. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroenceph. clin. Neurophysiol., 1978, 45: 302-304. Essick, G.K., Afferica, T., Aldershof, B., Nestor, J., Kelly, D. and Whitsel, B. Human perioral directional sensitivity. Exp. Neurol., 1988, 100: 506-523. Godaux, E. and Desmedt, J.E. Exteroceptive suppression and motor control of the masseter and temporalis muscles in normal man. Brain Res., 1975, 85: 447-458. Goldberg, L.J. Masseter muscle excitation induced by stimulation of periodontal and gingival receptors in man. Brain Res., 1971, 32: 369-381. Hart, B.A. Fractioned myotactic reflex times in women by activity level and age. J. Gerontol., 1986, 41: 361-367. Issler, H. and Stephens, J.A. The maturation of cutaneous reflexes studied in the upper limb in man. J. Physiol. (London), 1983, 335: 643-654. Lund, J.P. and Olsson, K.A. The importance of reflexes and their control during jaw movement. Trends Neurosci., 1983, 6: 95-98. Lund, J.P., Lamarre, Y., Lavigne, G. and Duquet, G. Human jaw reflexes. In: J.E. Desmedt (Ed.), Motor Control Mechanisms in Health and Disease. Raven Press, New York, 1983: 739-755. Mathewson, R.C. and Nava, P.B. Effects of age on Meissner corpuscles: a study of silver-impregnated neurites in mouse digital pads. J. Comp. Neurol., 1985, 231: 250-259. Matsuoka, S., Suzuki, H., Morioka, S., Ogawa, Y. and Kojima, T. Quantitative and qualitative studies of Meissner's corpuscles in human skin, with special reference to alterations caused by aging. J. Dermatol., 1983, 10: 205-216. Paulson, G. and Gottlieb, G. Developmental reflexes: the reappearance of foetal and neonatal reflexes in aged patients. Brain, 1968, 91: 37-52. Rowlandson, P.H. and Stephens, J.A. Maturation of cutaneous reflex responses recorded in the lower limbs in man. Dev. Med. Child Neurol., 1985, 27: 425-433. Sabbahi, M.A. and Sedgwick, E.M. Age-related changes in monosynaptic reflex excitability. J. Gerontol., 1982, 37: 24-32. Smith, A., Moore, C.A., Weber, C.M., McFarland, D.H. and Moon, J.B. Reflex responses of the human jaw-closing system depend on the locus of intra-oral mechanical stimulation. Exp. Neurol., 1985, 90: 489-509. Smith, A., McFarland, D.H., Weber, C.M. and Moore, C.A. Spatial organization of perioral reflexes. Exp. Neurol., 1987, 98: 233-248. Thexton, A.J. and McGarrick, J.D. Maturation of brainstem reflex mechanisms in relation to the transition from liquid to solid food ingestion. Brain Behav. Evol., 1984, 25: 138-145.