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.
Gr owing awareness of the po ten t i a l s ignif icance of changes in reflex funct ion that m a y occur with develop- men t and aging has mot iva ted numerous inves t igat ions of s tretch and cu taneous reflexes of the uppe r and lower l imbs in chi ldren and elder ly subjects (e.g., C la rkson 1978; Bawa 1981; Issler and Stephens 1983; Rowland- son and Stephens 1985; H a r t 1986). The results of these invest igat ions have s ignif icant impl ica t ions for under - s t and ing deve lop ing m o t o r skills and m o t o r perfor- mance in the elderly. Fu r the rmore , careful desc r ip t ions of h u m a n reflex func t ion are i m p o r t a n t c l inical ly and to theories of m o t o r control , which of ten inco rpo ra t e the idea that more complex m o t o r behaviors are bui l t on a founda t ion of pre-exis t ing reflex c i rcui t ry (e.g., Berkin- b l i t et al. 1986).
In cont ras t to reflexes of the l imbs, poss ib le changes in reflexes of the h u m a n o ra l -mo to r system over the life span have received l i t t le quant i t a t ive exper imenta l at- tent ion, a l though the re-emergence of ' p r im i t i ve ' or ' d eve lopmen ta l ' ora l reflexes in aged pa t ien t s has of ten been descr ibed (e.g., Paulson and Go t t l i eb 1968). This lack of exper imenta l a t ten t ion is surpr is ing in view of the fact that the h u m a n oral sys tem is endowed with m a n y reflex pa thways capab le of powerfu l modu la t i ng
Correspondence to: Dr. Anne Smith, Department of Audiology and Speech Sciences, Purdue University, West Lafayette, IN 47907 (U.S.A.).
effects on c ran iofac ia l m o t o n e u r o n pools , pa thways that are thought to p l ay a role in swallowing, mas t ica t ion , pos tu ra l s tabi l i ty , and possibly , speech p roduc t ion ( G o l d b e r g 1971; G o d a u x and D e s m e d t 1975; Cooke r et al. 1980; L u n d and Olsson 1983; Lund et al. 1983; Smi th et al. 1985).
In an earl ier s tudy f rom this l a bo ra to ry (Smith et al. 1985), responses of the j aw-c los ing sys tem to innocuous mechan ica l s t imuli app l ied to 8 in t raora l sites were examined in a g roup of 35 young adul t women. Re- sponses were measu red as changes in j aw-c los ing force and masse te r E M G s . The results ind ica ted a s t r iking spa t ia l o rgan iza t ion of reflex responses, with some in- t raora l sites p r o d u c i n g exci ta tory E M G responses and increases in j aw-c los ing force, and o ther sites p roduc ing suppress ions of E M G and decreases in the b a c k g r o u n d b i t ing force. In the present invest igat ion, we descr ibe the reflex responses p r o d u c e d in young girls and elder ly women b y s t imula t ion of 4 of the sites s tudied ear l ier in young adu l t women.
Methods
Subjects
Subjects were 25 girls aged 7 and 8 years and 25 w o m e n aged 7 0 - 8 0 years. F o r compara t ive purposes , results f rom an ear l ier s tudy (Smith et al. 1985), using essent ia l ly the same me thods of s t imula t ion and 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 miss- ing 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 displace-
ment 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 orthogo- nal 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 di- mension, in the vault of the boney palate.
AT - 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, approxi- mately 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. EMG signals were amplified (20 H z - 8 kHz bandpass) and full-wave recti- fied.
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 impres- sion material. This ensured that the same position on the force transducer was maintained during the test of each site of stimulation. The intermolar separation re- quired by the dimensions of the force transducer pro- duced an interincisal distance of approximately 1 cm.
Experimental procedure Subjects were seated in a dental chair with an ad-
justable 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
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 re- quired force level, and a total of 50 stimuli were de- livered. 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 ex- perimenter 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 reposi- tioned, 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 gen- erated 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 EMG records were displayed on a computer terminal. The peak-to-peak change in jaw- closing 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 EMG records from the right and left masseter muscles were judged as either containing a response, an
obvious change from the baseline EMG 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 EMG responses was measured with the aid of the simultaneous display of the cumulative sum for each EMG average (Ellaway 1978). The onset was selected as the first point where the averaged EMG deviated from the prestimulus baseline. The amplitude of the first component of EMG responses was measured by calcu- lating the definite integral of the voltage over the dura- tion 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 EMG response was longer than the prestimulus interval of 32 msec, the amplitude was calculated only from the first 32 msec of the EMG response.
Results
Control condition In this condition, subjects maintained either a 5 N
(children) or 10 N (elderly) biting force while stimula- tion 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 EMG 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 possi- ble observations or records for each group at each site is 50 (25 subjects × 2 averages/subject). Less than 50 were
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM
TABLE I
Percentage of average force records classified as response (R) and no response (NR).
121
Site Child Elderly X 2
No. of R N R No. of R NR records (%) (%) records (%) (%)
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. Chi- square statistics were calculated for each site to test for differences in proportions of responses and no re- sponses 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 in- cludes 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 de- creased force relative to the background biting force. Table II only indicates the direction of the initial com- ponent 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 stimula- tion of the tongue primarily produces increases in the background biting force. For the elderly, the predomi- nant 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 peak- to-peak changes in force following stimulation are ex- pressed 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.
EMG responses Table IV summarizes the numbers of EMG records
classified as showing a response or no response to stimulation. Data from the right and left masseter re- cordings are combined, so that for each group and each stimulation site, the total number of possible observa- tions is 100 (25 subjects x 2 repetitions of stimulation at each s i te /subject x 2 EMG recordings/subject). Chi- square statistics were used to test for differences be- tween 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 EMG records.
The graphs in Fig. 2 show the sign and latency of the first component of all of the EMG 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 Child Elderly
No. of Increase Decrease Mean No. of Increase Decrease Mean responses (%) (%) amp. responses (%) (%) amp.
The means and s t andard dev ia t ions of the peak- to -peak changes in
force expressed as a pe rcen tage of the b a c k g r o u n d b i t ing forces.
S t imula t ion Ch i ld ren Elder ly S tuden t ' s t
s i te
A P Mean 7.5 2.3 4.0 * *
S.D. 7.4 1.9
M P Mean 6.7 2.7 3.6 * *
S.D. 5.6 1.9
A T M e a n 6.1 2.2 3.2 *
S.D. 7.5 1.7
LT Mean 7.5 2.1 3.2 *
S.D. 10.0 1.9
* P < 0.01. * * P < 0.001.
two groups. The sign of the response is indicated by ' + , ' an excitation, or ' - , ' a suppression of the back- ground EMG activity. These symbols are plotted above ( + ) or below ( - ) a horizontal line representing the background EMG 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 EMG responses than the children. In addition, Fig. 2 demonstrates that the na- ture of the first component of the EMG responses of the children varied with different stimulation sites. In contrast, the first components of the EMG 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.
A. S M I T H ET AL.
The only stimulation site off-midline was LT. The EMG 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 excita- tory EMG responses, and these also showed a tendency for lateralization, that is, the short-latency excitation occurs more frequently in EMG responses recorded from the right side. Measurement of the amplitude of the first component of the EMG responses revealed that, for responses in which the first component was a suppression of ongoing EMG activity, the amplitude of the first component tended to be similar for the children and the elderly. For example, in response to AP stimu- lation, an initial suppression of activity was characteris- tic 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 -34%. When excitatory responses were observed, how- ever, 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%.
EMG responses also were classified as being simple or complex. Simple responses contained only one com- ponent, 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 com- plex responses. Stimulation of the lateral tongue re- suited in the largest percentages of simple responses; for children 47% of responses to LT stimulation were sim- ple 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 classif ied as responses (R) and no responses (NR). D a t a f rom r ight and left masse te r recordings have been combined .
Site Ch i ld Elder ly X 2
No. of R N R No. of R N R records (%) (%) records (%) (%)
A P 100 80 20 100 62 38 7.9 * MP 98 74 26 98 44 56 18.6 * *
Comparison of young adult (YA) responses with those of the elderly (E) and children (C)
Force responses. The percentages of force records 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
the 4 stimulation sites. The YA 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) com- parisons were not significant.
The means, standard deviations, and ranges of peak- to-peak amplitudes of force responses for each group
( I ) LI.I ( f ) Z o 13. ( I ) I l l at"
LL o 13:: LLI m
z
5
0
5
10 5
0
5 5
0
5 10
5
0
5 0
RIGHT MASSETER EMG RESPONSE
L a t e n c y ( m s )
I I t I i
CHILDREN
$
f . . . . . . . ,
t +; +1: ~___.,._. ,
I t , + + + + l " + + I + I "1" I | I I I I
LEFT MASSETER EMG RESPONSE
Latency (ms)
I - - - -+- - - L_
: - - :
A n t e r i o r P a l a t e 2 t + t I I I
:.~. M i d P a l a t e + ~ ' - + + + -~ _ _ - L _ _ I I ~''~ I I _ ~ ; I _ I
. . . . A n t e r i o r T o n g u e + + - ~ . + + +
.... t + + + + t + ++ +÷ I I I I I I - - - - - i - - --2-
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
l m m L - - ~
i 4 0 0 m s 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 dif- ferences 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).
EMG 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 observa- ble E M G responses, and the elderly had the fewest.
TABLE V
Mean peak-to-peak amplitude, standard deviation and range (in new- tons) of force responses of the children (C), young adults (YA) and elderly (E). The last column shows the mean expressed as a per- centage change from the background biting force.
Mean (N) S.D. (N) Range (N) Mean % change
C 0.41 0.42 0.06-2.70 8.2 YA 0.38 0.23 0.10-1.70 3.8 E 0.29 0.20 0.06-0.95 2.9
TABLE VI
Percentages of short-latency ( < 25 msec) EMG responses showing an excitation (EX) or suppression (S) for the children (C), young adults (YA), and elderly (E).
Stimulation C (%) YA (%) E (%) site
MP EX 39 9 0 S 61 91 100
AT EX 54 30 4 S 46 70 96
Chi-square statistics for group differences in propor- tions of r e sponse /no 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 re- sponses in the EMG, whether an excitation or a sup- pression, 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 short- latency 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 AT 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 short- latency excitation in the right masseter activity was the most common response, but the numbers of these re- sponses 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
REFLEXES OF THE H U M A N JAW-CLOSING 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 fol- lowed by a suppression of activity. With MP stimula- tion, 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 re- sponses, and 5% of E responses. The bot tom panel of Fig. 4, labeled E, is from one elderly subject and il- lustrates 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) oc- curred 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]
125
MP
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 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 st imulus probe.
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.
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 short- latency 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 dif- fered among the groups. Fig. 5 shows the E M G re- sponses of 3 children and 1 elderly subject to stimula- tion of the anterior palate. The two upper panels of Fig. 5, labeled C-1 and C-2, show the EMG 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) sup- pression and was observed in 23% of the EMG re- sponses of the children and in none of the EMGs of the
126 A. SMITH ET AL.
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 EMG 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 re- sponse, 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 EMG responses of the elderly.
Discussion
The results of the present investigation indicate that responses of the jaw-closing system to innocuous mech- anical 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 EMG 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 re- sponses 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 ab- solute amplitude of force responses increases when bit- ing 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 back- ground biting force. Even this attempt to normalize the
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 de- creased 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 stimula- tion sites (Table I), when percentages combined for the 4 sites were compared, the children were not signifi- cantly 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 fluctu- ations observed without tactile stimulation (control con- dition), 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 fol- lowing tactile stimulation had to exceed the value ob- served for that subject without tactile stimulation (con- trol 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 stimula- tion. 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 EMG responses present in the 3 groups. Children and the young adult group did not differ, while the elderly had a significantly lower percentage of EMG responses com- pared to the children and to the young adults. In fact, approximately one-half of the EMG records of the elderly were judged to contain no response. Only 30% of the force records of the elderly were classified as con- taining no response. This apparent discrepancy between force and EMG 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 tem- poralis muscles.
REFLEXES OF THE HUMAN JAW-CLOSING SYSTEM 127
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 pro- duced EMG responses with initial excitatory compo- nents, while stimulation of sites on the palate produced suppressions of ongoing EMG activity. Smith et al. (1985) presented arguments that suggest that the excita- tory responses are mediated by low threshold intra-oral mechanoreceptors, rather than arising from excitation of spindles in jaw-closing muscles. A number of investi- gators 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 re- flexes 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 me- chanical stimulation can produce relatively short-latency excitation of jaw-closing muscles, this terminology should perhaps be revised. We would suggest the re- sponses of jaw-closing muscles to intra- and peri-oral stimulation should be referred to simply as 'exterocep- tive responses.'
In addition to dependence on the site of stimulation, the sign of the initial component of exteroceptive re- sponses of jaw-closing muscles also appears to be de- pendent on the age of the subjects. In children, short- latency excitatory responses were common with mid- palate and anterior tongue stimulation (Table VI). The percentage of EMG responses with a short-latency exci- tatory component decreases with stimulation of these two sites in the young adult group. By age 70, short- latency 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 in- clude a reduction in the number of a certain type of intra-oral mechanoreceptor that gives rise to the excita- tory component, and changes in corticobulbar in- fluences that, over the life span, increasingly suppress the neural connections that mediate the early excitatory response.
The latency of spinal reflex responses has been con- sidered 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 EMG responses for other sites due to dif- ferences in the sign of the initial components. Re- sponses initiated by excitatory components tended to
occur earlier than those in which the initial response was a suppression (Fig. 2). Because the numbers of subjects showing the early excitatory components dif- fered 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 EMG 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. Inves- tigators 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 develop- mental 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 re- sults 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 developmen- tal trends in spinal reflexes, Rowlandson and Stephens (1985) stated, ' . . . reflex development is the companion
128 A. SMITH ET AL.
a n d no 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 skil ls ' (p.
431). S imi lar ly , the p r e s e n t resul ts sugges t tha t o r a l - m o -
tor ref lex d e v e l o p m e n t occurs in conce r t w i th d e v e l o p -
ing speech m o t o r skills. Sys t ema t i c changes in re f lex
responses also o c c u r in the p e r i o d f r o m y o u n g adu l t -
h o o d to the s even th d e c a d e of life. Th i s resul t i nd ica t e s
a c o n t i n u o u s e v o l u t i o n o f o ra l s e n s o r i m o t o r sys tems
t h r o u g h o u t the h u m a n l ife span.
F ina l ly , it shou ld be n o t e d that , in the p r e s e n t inves-
t iga t ion 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),
due to ev idence o f sex d i f f e r ences in ora l s enso ry capa -
bi l i t ies (e.g., Ess ick et al. 1988), we chose to s tudy
females only. It seems l ikely, however , tha t an essen-
t ia l ly s imi la r p a t t e r n of age - re l a t ed changes w o u l d char -
ac te r ize o r a l - m o t o r re f lexes in males .
This work was supported by Grants NS19173 and CD00559 from the National Institutes of Health.
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