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Craniofacial sequelae of lesions to facial and trigeminal motor nuclei in growing rats.

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Craniofacial Sequelae of Lesions to Facial and Trigeminal Motor
Nuclei in Growing Rats
Department ofBasic Sciences, University ofSouthern California School of
Dentistry, Uniciersity Park, MC-0641, Los Angeles, California 90089-0641
Motoneuron, Growth, Form, Neuromuscular,
Unilateral electrolytic lesions were made in the left-sidefacial
motor nucleus (FMNu) of six Sprague-Dawleyrats at 35 days of age in order to
correlate craniofacial sequelae with changed motoneuron function. Experimental and control rats were killed at 22, 32, 42, and 52 days postoperatively to
provide muscle weight, brain histology, and dry skull preparations for analyses. Dissection, muscle weight, motoneuron count, and osteometric data revealed that lesion-side facial and masticatory muscles were affected by the
lesions. Paired t-tests indicated that significant differences existed between
weights of experimental lesion- and nonlesion-side anterior digastric, temporalis, masseteric complex, and medial pterygoid muscles, numbers of facial and
trigeminal motoneurons, and several skeletal dimensions of the skull. Basicranial dimensions of experimental animals were least affected by the lesion,
whereas zygomatic arch, dorsal facial region, and mandibular condyle dimensions were most affected. Statistical analyses also detected significant differences between experimental and control groups for several skeletal dimensions
of the skull. Data indicated that damage to the trigeminal motor nucleus
(TMNu) was secondary to the primary lesion in the FMNu. Motoneurons
within the facial and trigeminal neuromuscular complexes (FNC and TNC)
play an important role in craniofacial growth and development.
Craniofacial form has been important to
students of human variation and evolution
at least since the days of Blumenbach (1795).
Despite the theoretical framework offered by
Wolff s law (1892), no significant experimental studies addressing the mechanical effects
of muscle upon skull form were accomplished
until Washburn (1946,1947) and his contemporaries (Horowitz and Shapiro, 1951, 1955;
Avis, 1959, 1961).
Muscles of facial expression (those innervated by cranial nerve VII,the facial nerve)
have been demonstrated to be of major importance in human craniofacial growth (Delaire and Chateau, 1977; DeIaire, 1978). In
addition, total paralysis of these muscles
combined with facial-nerve degeneration may
occur in 17%(Alberti and Biagioni, 1972) to
25%(Manning and Adour, 1972) of the total
pediatric Bell’s palsy patient population and
require surgical intervention before long-
0 1988 ALAN R. LISS, INC
term morphological and physiological sequelae manifest themselves (Jenkins et al.,
Previous studies have concentrated either
on resecting branches of the facial nerve and
studying morphologicallphysiological sequelae (Huber and Hughson, 1926; Washburn,
1946; Jarabak et al., 1949; Cammermeyer,
1963) or on correlating facial neuromuscular
changes with morphological alterations
(Miller and Chierici, 1982;Miller et al., 1982;
Vargervik et al., 1984). A major problem has
been to isolate the effects of the facial neuromuscular complex (FNC) on craniofacial
growth from those caused by sensory loss,
Received April 3, 1987; revision accepted September 21, 1987.
Address correspondence to Dr. Kenneth E. Byrd, Department
of Basic Sciences, USC School of Dentistry, University Park,
MC-0641, Los Angeles, CA 90089-0641.
tissue scarring, and circulatory interruptions
(Johnston, 1976) during actual facial-nerve
resections. This problem can be essentially
solved by electrolytically lesioning (Gardner
et al., 1980; Byrd, 1984) the facial motor nucleus (FMNu) within the brainstem.
The purpose of this investigation was to
determine the effects of alteration of the FNC
on craniofacial postnatal development by lesioning facial rnotoneurons (FMNe) within
the brainstem of actively growing rats. These
data therefore should approximate the craniofacial morphological sequelae resulting
from facial motor nucleus (FMNu) aplasia
(Walker, 1961) and/or progressive facial hemiatrophy (Chusid, 1979).
Detailed physiologic data (EMG and mandibular movement tracking a s in Byrd, 1984)
complementary to this study will be published elsewhere.
Six experimental and six control male
Sprague-Dawley rats underwent stereotaxic
surgery at 35 days of age. The animals were
induced with a n intramuscular injection of
“rat cocktail” (mixture of ketamine 100 mgl
ml, rompun 20 mglml, and acepromazine 10
mglml) in the amount of 0.01 ml per 10 g of
body weight. After induction, the animals
were positioned in a Kopf model 900 stereotaxic unit and maintained under general
anesthesia with halothane.
Surgical protocol was identical to that described in Gardner et al. (1980) and Byrd
(1984), in that a midline incision was made
over the sagittal suture; integument and
periosteum were reflected, and a small (4mm-diameter) hole drilled through the bone
to expose the dura mater. Both experimental
and control animals had a hole drilled directly over the left-side facial motor nucleus
(FMNu), according to general stereotaxic coordinates provided by Paxinos and Watson
(1982). Control animals had only their dura
exposed, and no lesions were produced in the
manner described by Gardner et al. (1980)
and Byrd (1984).
Experimental animals had unilateral electrolytic lesions (2 mA, 15 sec) placed in their
left-side FMNu in the manner described in
Byrd (1984) for the trigeminal motor nucleus
(TMNu). After piercing the dura, a Rhodes
NEX-100 concentric bipolar electrode was
slowly lowered while continuously stimulating at 1 pulse per sec at between 2 to 0.1
volts. The electrode descended in a n axis 1.9
mm to the left and 1.9 mm posterior to stereotaxic “ear bar zero.” FMNu targets were
located at a mean minimum stimulation
threshold of 0.41 & 0.31 volts with no trigeminal motor nucleus (TMNu) stimulation. At
no time during the electrode stimulation procedure for locating the FMNu target did the
trigeminal innervated muscles of mastication move; only facial muscles supplied by
the FMNu contracted during this procedure.
Electrodes were then placed a n additional
0.5 mm below that position eliciting the lowest threshold voltage causing facial muscle
response and lesions were produced with a
Grass direct-current lesion maker (2 mA, 15
Immediately after wound closure and
treatment with Betadine, both lesioned and
nonlesioned animals were given intraperitoneal injections of chloramphenicol sodium
succinate (0.25 ml) and were administered a n
oral suspension of chloromycetin palmitate
(1.0 ml) daily for 1 week postoperatively. In
order to document relative growth rates, both
experimental and control animals were
weighed to the nearest 0.1 g with Ohaus dial
scales on the day of lesioning and at 22, 32,
42, and 52 days postoperatively. Means and
standard deviations were calculated for these
Experimental and control animals were
killed at 22, 32 (two rats), 42, and 52 (two
rats ) days postoperative; transcardiac perfusion with 10% buffered formalin preceded by
a flush with physiological saline occurred a t
that time. Brains of lesioned and nonlesioned
animals were removed after transcardiac
perfusion for histological documentation of
lesion extent. Two additional rats were killed
and perfused immediately after lesioning in
order to confirm the locus of the initial FMNu
In order to document FMNu lesion effects
on the muscles of facial expression, these
muscles were dissected out en mass by means
of a n inverted “skin mask.” The following
muscles for both experimental and control
groups were then dissected free and weighed
to the nearest 0.01 g with Mettler dial scales
after storage in 70% ethanol: both left- and
right-side anterior digastric; posterior digastric; temporalis; masseteric complex = combined superficial, deep, maxillomandibularis,
and zygomaticomandibularis portions (Turnbull, 1970); and medial pterygoid. Unfortunately, lateral pterygoid proved impossible
to remove intact for weighing purposes and
TABLE 1. Osteological measurements used in this studv
Cranial measurements
1) Midline frontonasal suture to premaxillonasal suture (E-I, E-17
2) Maxillozygomatic suture to premaxillonasal suture (C-I,C’-I‘)
3) Maxillozygomatic suture to bregma (C-F, C‘-F)
4) Zygomaticosquamosal suture to premaxillofrontomaxillary suture (D-J, D’-J’)
5) Zygomaticosquamosal suture to midline frontonasal suture (D-E, D’-E)
6 ) Anteriormost incisoprernaxillary contact to anterior first molar (K-M, K‘-M’)
7) Anteriormost incisopremaxillary contact to occipitobullobasisphenoid contact (K-
R, K‘-R’)
Premaxillomaxillary suture to anterior first molar (P-M, P’-M’)
Premaxillomaxillary suture to maxillozygomatic suture (P-C, P’-C’)
Anterior first molar to maxillozygomatic suture ( M E , M‘-C’)
Anterior first molar to zygomaticosquamosal suture (M-D, M‘-D’)
Posterior third molar to maxillozygomatic suture (N-C, N’-C’)
Posterior third molar to zygomaticosquamosal suture (N-D, N’-D‘)
Posterior third molar to occipitobullobasisphenoidcontact (N-R, N’-R‘)
Posterior palatal spine to maxillozygomatic suture 1Q-C, Q-C’)
Posterior palatal spine to occipitobullobasisphenoidcontact (Q-R, Q-R’)
Occipitobullobasisphenoid contact to maxillozygomatic suture (R-C, R’-C‘)
Mandibular measurements
18) Gonial angle to superiormost incisorcorpus contact (S-T, S‘-T’)
19) Gonial angle to posterior third molar (S-W, S’-W‘)
20) Gonial angle to anteriormost condylar articular surface (S-Z, S’-Z’)
21) Superiormost incisorcorpus contact to posterior third molar (T-W, T’-W‘)
22) Superiormost incisorcorpus contact to superiormost coronoid process (T-Y, T’-Y’)
23) Superiormost incisorcorpus contact to anteriormost condylar articular surface (TZ, T‘-Z’)
24) Inferiormost incisorcorpus contact to superiormost coronoid process (U-Y, U’-Y’)
25) Inferiormost incisorcorpus contact to anteriormost condylar articular surface (Uz , U’-Z’)
26) Posterior third molar to anteriormost condylar articular surface (W-Z, W’-Z’)
27) Maximum mandibular height (MMH, MMH’)
28) Maximum condylar width (MCW, MCW‘)
29) Maximum condylar length (MCL, MCL’)
was not used. More superficial facial muscles, such a s the nasolabialis and dilator nasi,
were also not weighed because of their complex anatomy and delicate structure, which
prevented their intact removal for weighing
After removal of the previously described
muscles, the remaining tissue was cleaned
and dry skull preparations were made of both
lesioned and nonlesioned animals. A series
of 17 cranial and 12 mandibular measurements of the experimental and control groups
(see Table 1 and Fig. 1) were made for both
left and right sides, to the nearest 0.1 mm
with a Helios needle-point dial caliper.
The landmarks for three mandibular measurement points (S, Y, and Z in Fig. l) require further clarification: (1) point S (gonial
angle) was the posteriormost point of the
mandibular angle, (2) point Y (superiormost
coronoid process) was the highest point of the
coronoid process when the mandible was in
norma lateralis, and (3) point Z (anteriormost
condylar articular surface) was the most anterior contact of the condylar articular facet1
surface with the nonarticular surface of the
mandibular head (see Fig. 1). In addition,
maximum mandibular height (MMH) was
measured between two parallel planes: the
first, at the contact surfaces of the inferior
aspect of the mandible in norma lateralis; the
second, at point Y (superiormost coronoid
process). Maximum condylar length (MCL)
was measured between the anteriormost and
posteriormost articular surfaces of the mandibular condyle (anterior and posterior contacts between articular and nonarticular
surfaces of mandibular head). Maximum condylar width (MCW was measured between
the lateralmost and medialmost articular
surfaces of each mandibular condyle.
Histological documentation of lesion extent
was accomplished by first embedding the desired section of rat b r a i n (pons) after trans-
Fig. 1. Osteometric points used for this study. Primed
(9 points refer to right-side measurements. Refer to Table 1for complete description of points.
The purpose of motoneuron-count data was
to document differences between the left (lesioned) and right sides of both experimental
and control groups. To that end, actual motoneuron counts were made with the Optomax IV image analysis system and were
based on contrast differences between facial/
trigeminal motoneurons and their surrounding glial cells. The Optomax contrast detector setting was kept at a constant value of 83
during motoneuron-count procedures, and the
frame circle (area) counted was kept constant
between sides of the same histological section. Although every fourth 10-pm paraffin
section was mounted to facilitate data analysis for this study, a total of 374 facial and
294 trigeminal motoneuron counts using the
Optomax system provided sufficient data for
statistical analyses, as shown in Tables 2
and 3.
Statistical analyses of muscle weight, motoneuron count, and osteometric data consisted of means and standard deviations
calculated prior to tests of significance by
paired t-tests. Paired t-tests (Sokal and Rohlf,
1969) were used to test differences between
(1)left-lesioned and right-nonlesioned sides
and (2) experimental-lesioned and controlnonlesioned groups. These data are shown in
Tables 2-6.
Thirty-five-day-old rats were used instead
of younger animals because of their ability
to better recover from stereotaxic surgery.
Although 35-day-old rats are beyond their
period of most rapid craniofacial growth, sufficient craniofacial growth continues, particularly in their snout and facial regions (Baer
et al., 19831, to make analyses worthwhile.
For this study, the assumption was made
that any differences between the craniofacial
growth rates of animals killed a t 57, 67, 77,
and 87 days after birth were minimal.
cardiac perfusion and stabilization in 70%
ethanol. 10-pm-thick paraffin sections were
then cut, and every fourth section was
mounted and stained with Cresyl-violet stain
(LaBossiere and Glickstein, 1976). An estimate of both left- and right-side facial motoneurons (FMNe) and trigeminal motoneurons
(TMNe) was made with a n Optomax IV image analysis system. Both lesioned and
nonlesioned groups had their FMNu and
TMNu evaluated in this manner.
BehavioraUphyswlogical sequelae
Postlesion testing of experimental animals
revealed no lesion-side (1)vibrissae (whisker)
movement, (2) ear movement, or (3) nose
movement; all three are indicative of FMNu
damage. In addition, no lesion-side ear tremble or eye blink reflex (Fig. 2) could be elicited; lesion-side trigeminal sensory supply
was largely intact, as demonstrated by
touching the lesion-side vibrissae of the experimental animals and eliciting responses
TABLE 2. Numbers of facial motoneurons @MNe) detected in experimental and
control groups (X f S.D.)
(n = 19)
0.69 f 1.95
(n = 26)
4.74 k 7.98
(n = 31)
53.08 f 20.05
(n = 13)
83.21 t 30.66*
(n = 19)
69.12 f 28.66*
(n = 26)
72.81 rt 31.12*
(n = 31)
87.62 5 37.15*
(n = 13)
66.95 f 29.78
(n = 22)
55.94 f 31.14
(n = 32)
43.88 f 18.28
(n = 25)
39.05 f 27.73
(n = 19)
68.68 f 31.59
(n = 22)
55.31 f 38.44
(n = 32)
43.88 f 18.24
(n = 25)
41.74 f 26.06
(n = 19)
*Left significantly different from right P 6 .01
TABLE 3. Numbers of trigeminal motoneuron_s(TMNe) detected in experimental and
control groups (X f S.D.)
Days postop.
7.90 f 6.68
(n = 20)
6.11 t 6.96
(n = 19)
0.16 f 0.62
(n = 25)
25.28 & 11.89
(n = 18)
58.20 f 38.36*
(n = 20)
58.47 f 30.07*
(n = 19)
47.04 f 22.12*
(n = 25)
73.22 f 20.17*
(n = 18)
*Left significantly different from right P
31.06 15.08
(n = 17)
29.77 f 16.90
(n = 22)
25.75 f 10.05
(n = 8 )
27.06 f 16.31
(n = 18)
32.65 f 15.35
(n = 17)
30.50 f 18.95
(n = 22)
27.75 f 9.94
(n = 8)
23.67 rt 17.99
(n = 18)
< .01.
from them. These behaviors were present in
experimental animals immediately after surgery and were present throughout the course
of the study.
Despite lesion-side (left) “mouth droop” and
nasal deviation to the nonlesion side (right),
experimental rats fed themselves efficiently
immediately after recovering from surgery.
Within 3 to 4 days postlesion, however, it
was observed that the experimental rats appeared to have difficulty in eating their norma1 rat pellets. Both experimental and
control rats were then provided water-softened pellets and a paste made of powdered
pellets and water. Approximately 13 days
postlesion, hypereruption of maxillary and
mandibular incisors of the experimental rats
necessitated their reduction so that they
could continue to feed and gain weight. Both
experimental and control rats were fed and
watered ad libitum, but experimental rats
were not a s rapid in their weight gain, cornpared with their control counterparts.
The body weights (x k sod-)for experimental and Control groups a t the time of lesion-
ing were, respectively, 153.1 +_ 7.1 g and
150.2 f 7.7 g. Presacrifice body-weight gains
of experimental rats at 22, 32, 42, and 52
days postoperatively were 28.7 f 27.7 g, 68.5
f 16.9 g, 116.5 22.1 g, and 175.9 f 14.9 g,
respectively. Presacrifice body-weight gains
of control animals a t 22, 32,42, and 52 days
postlesion were 134.8 & 9.4 g, 161.6 f 6.2 g,
180.9 k 6.7 g, and 280.6 f 22.2 g, respectively. These weight-gain differences between experimental and control groups
reflect the physiological and morphological
sequelae of the FMNu lesions in the lesioned
Facial muscles
Lesion+ide facial muscles were
and less robust than their nonlesion-side
counterparts. The lesion-side nasolabialis
et al., 1983, which
whiskers, nose, and upper lip, was much
smaller than the nonlesion-side muscle, as
was the lesion-side zygomaticus, platysma,
terior digastric of the control animals were
significantly ( P < .01) heavier than their
experimental antimeres (Table 4).
Left (lesion-side) temporalis, anterior digastric, masseteric complex, and medial pterygoid were significantly ( P < .05, < .01)
lighter than right ones in the experimental
animals (Table 4).Experimental posterior digastric was not significant ( P < 20). No significant left-right differences were detected
in the control animals (Table 4).Despite its
apparent atrophy, as shown in Figure 5, posterior digastric did not show any significant
weight difference between lesioned and
nonlesioned sides of experimental animals.
Left-side posterior digastric in control animals was significantly (P < .01)heavier than
its experimental counterpart, however.
The facts that all five left-side control muscles were significantly heavier than their ex-
Fig. 2. Eye blink reflex test in FMNu-lesioned animal
at 52 days postoperative. Note normal blink reflex for
nonlesion-side eye (top) and absent blink reflex for lesion-side eye (bottom).
and mentalis. Lesion-side orbicularis oris was
also paler and less robust than on the nonlesion-side. Deeper dissections prior to dry skull
preparations also revealed a significant color
difference between lesion- and nonlesion-side
buccinator muscles in the experimental animals (Fig. 3). Lesion-side buccinators appeared both paler and thinner than their
nonlesion-side counterparts.
Masticatory muscles
Figures 4 and 5 demonstrate that there
was not only atrophy of lesion-side posterior
digastric (innervated by facial nerve), but also
considerable wasting of lesion-side muscles
of ast tic at ion (innervated by trigeminal
nerve). Table 4 indicates statistically significant differences between experimental and
controlmuscleweights for left and right ternp o r a b anterior digastric, and Illasseteric
complex. Left-side medial pterygoid and pos-
Fig. 3. Temporalis and buccinator muscles in FMNulesioned animal at 32 days postoperative. Contrast appearance of nonlesion-side muscles (top) with lesion-side
temporalis and buccinator muscles (bottom).Buccinator
muscles are indicated by arrows. Note (1)robust temporalis on nonlesion side (top) and (2) pale buccinator on
lesion side (bottom).
TABLE 4. Muscle weights of exnerimental and control eroum lX
Ant. digastric
Post. digastric
Masseteric complex
Medial pterygoid
0.12 k 0.02
(n = 6)
0.13 k 0.01
(n = 6)
0.29 f 0.22
(n = 6)
0.76 i 0.56
(n = 6)
0.18 +_ 0.06
(n = 5)
0.16 k 0.02**
(n = 6)
0.14k 0.02
(n = 6)
0.53 0.19**
(n =6)
1.14 ir 0.37*
(n = 6)
0.25 +_ 0.04**
(n = 5)
*Left significantly different from right P < .05.
**Left significantly different from right P < .01.
+ControlSignificantly different from experimentals P
+ S.D.P )
0.20 f 0.02'~
(n = 6)
0.15 f O.Olr
(n = 6)
0.91 & 0.18+
(n = 6)
1.80 0.33$
(n = 6)
0.29 & 0.07T
(n = 6)
0.21 & 0.Olt
(n = 6)
0.15 f 0.02
(n = 6)
0.90 k 0.17t
(n = 6)
1.81 i 0.35'
(n = 6)
0.28 f 0.07
(n = 6)
< .01.
perimental antimeres and that only three
right-side control muscles were significantly
heavier than their experimental counterparts suggest that the lesion's effect was
greater on left-side muscles of the experimental animals (see Table 4). In addition, the
significant differences between left- (lesion)
and right-side temporalis, anterior digastric,
masseteric complex, and medial pterygoid
muscles in the experimentals point to a major effect caused by the lesion.
Facial and trigeminal motoneurons
Histological sections of the two rats killed
and perfused immediately after lesioning revealed (1) the accurate placement of the electrolytic lesion into the FMNu and (2) no
apparent damage t o the TMNu. Although
the FMNu was indeed the primary lesion site
in the experimental animals (see Figs. 6 and
71, TMNu damage was substantial at 22 and
32 days postoperatively (Fig. 7 and Table 3).
The mean size of the primary FMNu lesion
(Fig. 6) for all six experimental animals was
approximately 645 ( f131) pm wide by 1438
(+257) pm high. No lesion-side FMNe were
detected at 22 days postoperatively in the
experimental group and few were detected a t
32 and 42 days postoperatively (Table 2).
However, very few lesion-side TMNe were
detected a t 42 days postoperatively (Table 3).
~ ~ ~ iF M~N ~~
and -T M~ N ~iof experimend ~
tal animals were si@ificantly ( p .O1) fewer
than nonlesion-side motoneurons, but no significant differences were detected between
sides of control animals (Tables 2 and 3). The
greater left-side FMNe and TMNe counts for
experimental animals at 52 days postoperatively probably reflect a relatively poor lesion for those particular animals; their
Fig. 4. Masticatory muscles of FMNu-lesionedanimal
at 22 days postoperative. Note robust temporalis and
masseter muscles of nonlesion side (top), compared with
atrophied appearance of lesion-side muscles (bottom).
histological sections showed most gliosis dorsal and slightly caudal to the FMNu proper.
However, statistical analyses of these motoneuron-count data strongly suggest that the
Fig, 5, Superior (top) and inferior (bottom) views of
animal shown in Fig. 4.Notice relative atrophy of lesionside temporalis (top) and posterior digastric muscles
(bottom), as indicated by arrows.
major effect of the unilateral FMNu lesion
was on the lesioned (left) side.
Osteometric analyses
Figures 8 and 9 show the extent of skeletal
alterations due to the effects of the lesion.
Notable cranial alterations in the experimental animals included (1)deviation of nasal and premaxillary bones to the nonlesioned (right) side, (2) bone loss in the
nonlesion-sideinfraorbital region, and (3) less
robust lesion-side zygomatic arches (see Fig.
8). Mandibular alterations of experimental
animals included (1)reduced size of lesionside condyles, coronoid processes, and gonial
angles and (2) smaller lesion-side mandibular corpus (see Figs. 8 and 9).
Tables 5 and 6 reveal that the greatest
effect of the unilateral FMNu lesion upon
experimental animals occurred for cranial
measurement C-I and mandibular measurements W-Z, maximum condylar width, and
maximum condylar length (refer to Fig. 1 for
orientation). Paired t-tests detected no significant differences between left and right sides
in the control animals for either cranial or
mandibular measurements. However, controls were significantly ( P < .05, < .01) different from experimentals for all cranial and
mandibular dimensions except left-side C-I
and T-Z and right-side D-J, D-E, and T-Z.
Only mandibular dimension T-Z displayed
no significant differences between experimental and control groups (see Fig. 1, Tables
5 and 6).
Several cranial measurements that provided growth vector information for the basicranium (K-R, P-M, P-C, M-C, and M-D) did
not display any significant differences between lesioned and nonlesioned sides of experimental animals (Table 5). The cranial
dimension C-I is of particular interest because the experimental nonlesion-side(right)
was significantly ( P < .01) greater than its
control counterpart; C-I was the only cranial
or mandibular dimension in which the experimental mean value was greater than the
control value.
Mandibular dimension W-Z (Table 6) was
unusual in that the significant difference ( P
< .O1) between right-side
Control samples was €Water than that between left-side experimental and control
groups ( P < .05). The significantly ( P < .01)
greater value of the experimental left-side
W-Z dimension, compared with its experimental right-side, probably reflects the
shorter condylar-length value shown for the
experimental left-side maximum condylar
length (MCL)dimension (see Fig. 1,Table 6).
The fact that both lesion-sidecondylar width
(MCW) and length (MCL) dimensions were
significantly ( P < .01) smaller than nonlesion-side ones in experimental animals suggests a major effect of the lesion on condylar
Summary of osteometric analyses
In general, control animals displayed significantly greater dimensions than did experimentals for (1)cranial measurements except
C-I and (2) all mandibular measurements,
with one exception: T-Z. The only significant
differences between left and right sides of
experimental animals occurred for (1) dimen-
Fig. 6. Nonlesion-side (large arrow) and lesion-side to lesion-side facial motoneurons (FMNe), compared with
(small arrow) facial motor nuclei (FMNu) of lesioned nonlesion-side FMNe.
animal at 32 days postoperative. Notice massive damage
Fig. 7. Nonlesion-side (large arrow) and lesion-side
(small arrow) trigeminal motor nuclei (TMNu) of animal
shown in Fig. 6; section is approximately 1,320 pm anterior to that shown in Fig. 6 . Notice (1)the fewer lesion-
side trigeminal motoneurons (TMNe), compared with
their nonlesion-side counterparts, and (2) the absence of
massive damage to lesion-side TMNu, contrasted with
that shown in Fig. 6 for the FMNu.
(Figs. 6 and 7, Tables 2 and 3) indicated that
the FMNu was the primary lesion site;
TMNu damage, although substantial, was
apparently secondary to the initial lesion
produced in the FMNu.
The anteroposterior distance between histological sections of the same animal shown
in Figures 6 and 7 is approximately 1,320
pm. As documented in Figure 48 of Paxinos
and Watson (1982), the anteroposterior distance between caudalmost TMNu and the
FMNu lesion site used in this study (1.9 mm
lateral and 1.9 mm posterior to ear bar zero)
is a t least 1,200 pm. In addition, at the coordinates of 1.9 mm lateral to ear bar zero,
inferiormost TMNu is approximately 900 pm
Fig. 8. Superior views of crania (top) and mandibulae
(bottom) of FMNu-lesioned animals at 22, 32, and 42
days postoperative (left to right). Notice progressive reduction of bone in infraorbital region (arrows in top
plate), slight rostra1 deviation toward nonlesion (right)
side, and progressive reduction in size of lesion-side (left)
mandibular condyles (arrows in bottom plate).
sions involving the zygomatic arch and dorsal facial region in the cranium (C-I) and (2)
dimensions involving the articular surfaces
of the mandibular condyle (W-Z, maximum
condylar width, maximum condylar length).
Lesion effectiveness
Data presented here indicate that unilateral lesions of the FMNu caused significant
alterations of the craniofacial complex. The
damage to the TMNu and the muscles of
mastication was unexpected because (1) no
observable stimulation of TMNe occurred
during the lesioning process and (2) a small
(2-mA, 15-sec)
lesion was used.
Histological documentation of lesion damage
Fig. 9. Superior (top) and inferior (bottom) views of
mandible of FMNu-lesioned animal a t 42 days postoperative. Notice lesion-side (left) condylar reduction, incisor
deviation, and mandibular corpus reduction relative to
nonlesion (right) side.
TABLE 5. Cranial dimensions ofexperimental and control animals
13.35 & 0.88
(n = 6)
19.95 f 1.68
(n = 6)
13.07 & 0.87
(n = 3)
17.32 f 1.75
(n = 6)
i8.03 L 1.48
(n = 6)
13.82 f 0.76
(n = 6)
31.52 f 2.11
(n = 6)
5.52 f 0.55
(n = 6)
14.92 f 1.40
(n = 6)
9.92 f 0.99
(n = 6)
15.28 f 1.07
(n = 6)
6.87 f 1.17
(n = 6)
9.67 f 1.11
(n = 6)
10.25 f 0.92
(n = 6)
10.02 f 1.12
(n = 6)
8.70 f 0.98
(n = 6)
13.42 f 1.36
(n = 61
13.33 f 0.98
(n = 6)
22.12 f 1.81*
(n = 6)
13.47 f 1.25
(n = 3)
18.13 f 1.85
(n = 6)
i8.83 f 1.62
(n = 6)
13.72 f 0.78
(n = 6)
31.57 f 2.25
(n = 6)
5.63 & 0.67
(n = 6)
14.93 f 1.39
(n = 6)
10.20 f 0.98
(n = 6)
15.55 f 1.05
(n = 6)
6.90 f 0.89
(n = 6)
9.68 k0.68
(n = 6)
10.27 f 1.08
(n = 6)
10.20 fO.91
(n = 6)
8.52 & 1.11
(n = 6)
13.62 f 1.03
(n = 6)
(x f S.D. mm)
14.55 f 0.84'
(n = 6)
20.40 f 1.07
(n = 6)
16.32 f 0.85'
(n = 5)
18.65 f 1.24'
(n = 6)
19.45 f 1.12'
(n = 6)
15.18 f 0.94'
(n = 6)
34.40 f1.79'
(n = 6)
6.27 f 0.50'
(n = 6)
16.70 f 0.80'
(n = 6)
11.35 f 0.49'
(n = 6)
17.02 f 0.80'
(n = 6)
8.30 f 0.36'
(n = 6)
11.32 f 0.66'
(n = 6)
11.88 f 0.88'
(n = 6)
11.40 f 0.33'
(n = 6)
9.68 f 0.70'
(n = 6)
15.10 f 0.55'
(n = 6)
14.55 k0.82'
(n = 6)
20.47 f 1.07t
(n = 6)
16.38 f 0.84'
(n = 5)
18.60 f 1.24
(n = 6)
19.44 f 1.08
(n = 6)
15.15 f 0.94'
(n = 6)
34.41 f 1.75'
(n = 6)
6.28 f 0.52'
(n = 6)
16.68 f 0.80'
(n = 6)
11.33 f 0.52t
(n = 6)
17.00 f 0.77'
(n = 6)
8.25 f 0.32'
(n = 6)
11.35 f 0.5gt
(n = 6)
11.88 f 0.87'
(n = 6)
11.43 f 0.38t
(n = 6)
9.68 f 0.68'
(n = 6)
15.08 f 0.52'
(n = 6)
*Left significantly different from right P < .01
+Controlssignificantly different from experimentals P 4 .01.
above and 1,800 pm anterior to the FMNu
lesion site used in this study (Paxinos and
Watson, 1982). Because the mean FMNu lesion width (and assumed anteroposterior extent) was approximately 645 (k131) pm and
because its anteriormost extent occurred at
least 400 pm posterior to lesion-side TMNu,
it does not appear that the initial lesion
caused the secondary TMNu damage documented in this study. Histological sections of
the two rats killed and perfused immediately
after lesioning confirmed the accurate placement of the initial FMNu lesion and revealed
no apparent damage to the TMNu (see the
section on results; in addition, previously reported postlesion behavioral data in that section also support this interpretation).
One possible explanation for the apparent
secondary damage to the lesion-side TMNu
might be delayed vascular effects. Secondary
hemorrhage can cause severe damage to pontine nuclei within the brainstem and can
create both facial palsies (Milland-Gublerand
Foville's Syndromes) and jaw-muscle paralysis (alternating trigeminal hemiplegia) as described by Chusid (1979).The delayed TMNu
sequelae observed in this study therefore
could be due to neurovascular microhemorrhages caused by the initial FMNu electrolytic lesion. One way to determine if the
delayed trigeminal effects are due to hemorrhagic events resulting from the FMNu electrolytic lesions would be to produce chemical
lesions in the FMNu by microiontophoretic
techniques using ibotenic acid (IBO).IBO has
the distinct advantage of producing neuronal
death without destroying adjacent structures
(Markowska et al., 1985). Preliminary research involving microinjections of IBO into
growing rat TMNu has just started (Byrd
unpublished data); no TMNu-FMNu interactions have yet been observed. Clearly, more
discrete and motoneuron-specific lesioning
techniques are needed to fully understand
the data presented here. The replication of
this experiment using identical and smaller
size electrolytic lesions, combined with physiological data previously described, is in progress and should answer some of the specific
questions raised here.
A neurophysiological basis for TMNu damage by a small electrolytic lesion placed in
the FMNu may be the presence of reticular
formation projections between the facial and
trigeminal motor nuclei in the rat (Travers
and Norgren, 1983). These projections are
probably involved with the masticatory a n d
or facial CPGs. It is possible that the eledrolytic lesions produced in this study damaged
not only the FMNu but also the reticular
formation projections between the FMNu and
TMNu; the subsequent damage to the TNC
could then be accounted for by transneuronal
degeneration (Brodal, 1981) even though no
actual TMNe were stimulated during the actual lesioning procedure.
Masticatory muscle weight data (Table 4)
confirm the histological damage to the TMNu
shown in Table 3. Previous studies lesioning
the TMNu in experimental animals have
documented muscular and skeletal alterations similar to those described here (Gardner et al., 1980; Phillips et al., 1982; Byrd,
1984). The essential lack of statistically significant weight differences for the posterior
digastric of experimental animals (Table 4)
suggests that despite massive damage to the
FMNu (Table 2, Figs. 2, 3, and 6), the motoneuron pool directly supplying the posterior
digastric was little affected by the initial lesion. Posterior digastric motoneurons in the
rat are located within an accessory facial motor nucleus immediately dorsal to the FMNu
proper (Matsuda et al., 1979; Szekely and
Matesz, 1982; Shohara and Sakai, 1983). Because the initial FMNu lesion was placed an
additional 0.5 mm below that position eliciting the lowest threshold voltage in the main
FMNu (see the section on materials and
methods), lesion effects were most pronounced in the main FMNu. This explains
why the posterior digastric, with motoneurons in the accessory facial motor nucleus,
was relatively unaffected by the initial
FMNu lesion compared to other facial muscles with their FMNe located in the FMNu
It should be noted that many of the differences between experimental and control animals documented in Tables 2, 5, and 6 may
be due to the relatively poor weight gain of
the experimentals compared with that of
their control counterparts (see the results
section). This unavoidable sequela of producing electrolytic lesions suggests that differences between left (lesion) and right (nonlesion) sides of experimental animals should
be weighted more than differences between
experimental and control groups during any
interpretations of unilateral FMNu lesion effects on craniofacial form.
CNS lesion studies of the trigeminal system of the rat include those by Frank and
Karli (1962), Pimenidis and Gianelly (1977),
and Behrents and Johnston (1984). All these
studies concentrated on the trigeminal sensory system, although it appears that morphological alterations resulting from V3
motoneuron axonal damage occurred in each
investigation. It is a major problem to discern the role of the trigeminal neuromuscular complex (TNC)in craniofacial growth and
to separate effects resulting from sensory
neurons from those resulting from motoneuron activity. In this study, the sensory component of the TNC was largely unaffected by
the lesion, as determined by the postoperative reflex testing and behavioral observations documented in the section on results.
The absence of eyeblink reflex was apparently due to damaged FMNe innervating the
orbicularis oculi muscle because touching lesion-side vibrissae elicited behavioral responses from experimental animals.
A distinction should be made between
“neurotrophic” and “neuromuscular” effects
resulting from lesion studies. Following the
definitions provided by Behrents and Johnston (1984), neurotrophic effects would be
those resulting from a disturbance or interuption of a nutritive or sustaining substance
within the nervous system, possibly biochemical in nature. Neurornuscular effects, on the
other hand, would be due to a disturbance or
interruption of mechanical forces between
bone, muscle, and cartilage that are modulated by CNS sensorimotor systems. Data
presented here and by previous researchers
(Frank and Karli, 1962; Pimenidis and Gianelly, 1977; Sarnat et al., 1977; Gardner et
al., 1980;Behrents and Johnston, 1984; Byrd,
1984) suggest that those studies that lesion/
resect sensory portions of the TNC would
largely alter supposed neurotrophic effects;
TABLE 6. Mandibular dimensions of experimental and control animals (52 f
23.98 f 1.93
(n = 5)
9.98 1.62
(n = 6)
7.73 f 0.97
(n = 6)
14.44 f 0.43
(n = 5)
19.54 f 1.45
(n = 5)
22.22 0.90
(n = 5)
18.72 1.18
(n = 5)
20.54 f 1.12
(n = 5)
8.87 k 0.47
(n = 6)
11.90 & 0.99
(n = 6)
1.08 0.41
(n = 6)
2.42 f 0.44
(n = f 3
25.07 k 1.46
(n = 6)
10.57 f 1.00
(n = 6)
7.83 f 0.74
(n = 6)
14.60 0.36
(n = 6)
19.83 k 0.96
(n = 3)
21.93 f 1.36
(n = 6)
18.50 k 0.90
(n = 3)
19.92 f 1.44
(n = 6)
8.25 0.93*
(n = 6)
11.80 f 0.53
(n = 3)
1.50 f 0.21*
(n = 6)
3.15 f 0.19*
in = 6)
26.70 f 1.26tt
(n = 6)
12.13 5 0.73''
(n = 6)
9.42 k 0.35"
(n = 6)
15.08 k 0.59++
(n = 6)
21.98 k 0.91tt
(n = 5)
22.92 k 1.12
(n = 6)
21.24 f 0.84tt
(n = 5)
21.60 k 0.65tt
(n = 6)
9.21 0.58'
(n = 6)
13.58 f 0.61''
(n = 5)
1.73 f 0.05'+
(n = 6)
3.85 f 0.24++
26.67 1.24'+
(n = 6)
12.10 f 0.75'1
(n = 6)
9.40 k 0.2gtt
(n = 6)
15.13 0.67''
(n = 6)
21.63 k 0.81t'
(n = 4)
22.83 f 1.06
(n = 6)
20.93 k 0.54'?
(n = 4)
21.65 0.68"
(n = 6)
9.23 k 0.56+'
(n = 6)
13.57 f 0.65'+
(n = 5)
1.75 k 0.05tt
(n = 6)
3.85 0.18"
in = 6 )
"Left significantly different from right P < .01.
+Controls significantly different from experimentals P < .05.
ttControls significantly different from experimentals P < .01.
likewise, those studies that lesionhesect motor portions of the TNC would alter those
neuromuscular effects. The problem, it
seems, is largely a methodological one: better
discrimination of sensory and motor components of the TNC in lesionhesection studies
should allow a better understanding of the
respective roles played by both neurotrophic
and neuromuscular factors in craniofacial
Although neurotrophic substances are defined as "nonnerve impulse," maintainancel
homeostatic agents found in both motor and
sensory nerves (Gutmann, 19761, these debates do not detract from the value of such
studies; rather, they indicate that there is
much interaction between sensory and motor
components not only of the TNC, but of all
motor systems in the craniofacial complex. A
pressing question is, What are the relative
contributions of the respective sensory and
motor systems to craniofacial growth and
Neurophysiological factors
Byrd (1984) documented that electrolytic
lesions of the TMNu do not completely sup-
press masticatory muscle activity in growing
guinea pigs; in addition, profound morphological alterations of the craniofacial complex were produced by such lesions. It was
therefore suggested that muscular paresis
and altered neuromuscular activity patterns
can produce skeletal changes in the craniofacial region: total paralysis is not required
for significant changes (Byrd, 1984). Data
presented here also indicated that significant
musculoskeletal alterations occurred without complete destruction of facial and trigeminal motor nuclei in young rats (Tables 2
and 3).
Data presented here also suggest the presence of neurophysiological interactions between the FMNu and TMNu that have direct
and indirect effects on craniofacial growth in
the laboratory rat. The observed secondary
damage to the TNC resulting from primary
lesions in the FMNu is of interest because
similar-size electrolytic lesions (2 mA, 15 sec.)
in guinea pigs (Gardner et al., 1980; Byrd,
1984) do not produce secondary damage to
the FMNu. This difference between guinea
pigs and rats may be due to their physical
size differences; there is an interval of ap-
proximately 1,600 pm between caudalmost
TMNu and rostralmost FMNu in guinea pigs
(Byrd, unpublished data), whereas the same
distance in rats is approximately 1,100 pm
(Paxinos and Watson, 1982). In addition, significantly different neurophysiological and
neuroanatomical mechanisms exist between
different mammalian taxa (Byrd, 1985).
If craniofacial growth is indeed correlated
with muscle attachment sites but not necessarily with growth of individual muscles
(Nakata, 1981), it would seem that muscle
activity (EMG) patterns are of prime importance in the determination of skull form.
Both tonic and phasic EMG activity patterns
have been studied in this regard (Miller and
Chierici, 1982; Miller et al., 1984; Byrd,
1984). These activity patterns are currently
thought to be initiated by at least one, and
possibly by several, central pattern generators (CPG) within the reticular formation of
the pontine brainstem (Luschei and Goldberg, 1981). In this study, then, CPGs involved with both facial and trigeminal motor
nuclei and their respective muscular terminations would have been affected by the produced lesion. Physiological data are currently
being collected to test this hypothesis (Byrd,
in preparation).
Role of the facial neuromuscular complex
The facial neuromuscular complex (FNC)
is defined here as (1)the muscles innervated
by cranial nerve VII; (2) nerve VII and its
branches; (3) afferent and efferent nerve fibers to those muscles supplied by VII; and (4)
nuclei within the CNS giving rise to those
fibers. Because both facial and trigeminal
neuromuscular complexes were altered in
this study, the relative contributions of each
to the observed morphological alterations
must be determined by their respective muscle attachment sites and by research reported
by previous investigators.
Both Washburn (1946) and Jarabak et al.
(1949) resected the facial nerve at the stylomastoid foramen in growing rats. They both
observed deviation of the premaxillary and
nasal bones to the nonlesion side. This agrees
with the results of this study in which nonlesion-side snout deviation and bone loss in the
nonlesion-side infraorbital region were detected (Fig. 8). Washburn (1946) further asserted that the mechanism involved seemed
to be “purely mechanical.” Assuming that
mechanical forces generated by facial muscles are capable of producing both rostral
deviation and infraorbital region bone loss
(as shown in this study), which muscles could
have caused those morphological changes?
Meinertz (1942) describes in great detail
the facial musculature of the rat and provides the answer to this question. The region
of nonlesion-side infraorbital bone loss shown
in Figure 8 may be due to the unbalanced
activity of the nonlesion-side nasolabialis, dilator nasi, maxillonasialis, and bucconasolabialis muscles that attach to that area
(Meinertz, 1942). In this sense, the nonlesionside infraorbital bone loss shown in Figure 8
may be a n example of “flexure-drift” bone
modeling (Frost, 1963, 1983) caused by unchecked activity of these nonlesion-side rostral muscles. All these muscles are supplied
by FMNe and are continuously active in the
“whisker-moving” activity of rats and other
rodents (Wineski, 1983). It would appear,
then, that the major effect of the FMNu lesion on the experimental rats’ facial skeleton
was primarily rostral; this is confirmed by
statistical analyses of osteometric data (dimensions C-I, D-J, and D-E in Fig. 1, Table
If control animals are also considered, facial dimension K-M was also affected by the
altered FNC (see Table 5). Based on masticatory-muscle attachment sites, as outlined by
Turnbull (19701, it appears that all remaining cranial and mandibular skeletal alterations in this study were due to alteration of
the TNC. This is consistent with skeletal sequelae following TMNu lesions in previous
studies (Gardner et al., 1980; Phillips et al.,
1982; Byrd, 1984).
Neuromuscular effects
As described earlier, it appears that effects
of the FNC on the skull are secondary to
those of the TNC; this statement is substantiated by physiological data from hemifacial
microsomia patients (Vargervik and Miller,
1984). It was found that EMG signals from
facial muscles (FNC) were predominantly
normal in all manifestations of hemifacial
microsomia, whereas masticatory muscles
(TNC) could demonstrate abnormal EMG
patterns in any malformation type. Furthermore, neuromuscular effects on the craniofacia1 skeleton by the TNC have recently been
identified for plagiocephaly (Kreiborg et al.,
1985) and skull shape in general (Weijs and
Hillen, 1984).
Perhaps the most important finding of this
study is that damage to the CNS can effect
massive changes in the TMJ (Figs. 8 and 9,
Table 6). The lesion-side condylar changes
shown in Figures 8 and 9 may be an example
of regressive modeling of the TMJ (Moffett,
1966) if there was actual movement of the
condylar articular surface away from the articular cavity; future histological studies
should resolve the question. It is assumed
that the neuromuscular effects on the lesionside condyles were those modulated by an
altered (postlesion)TNC, because the lesionside lateral pterygoid muscles (although not
weighed) appeared smaller and paler than
nonlesion-side ones. This finding agrees with
Petrovic’s view that the lateral pterygoid
muscle plays a major role in normal condylar
and subsequent mandibular growth (Petrovic
et al., 1975; Oudet and Petrovic, 1978).
Paired t-tests between lesion- and nonlesion-side condyles of experimental animals
displayed significant differences for both
maximum condylar length and maximum
condylar width (Table 6). Actual values o f t
also demonstrated that the greatest difference between condylar dimensions of experimental and control animals was for condylar
length (x f s.d. t value of 15.14 0.69 at 10
d.f.) and not width (2 + s.d. t value of 7.48
1.61 at 10 d.f.). However, Herring and Lakars
(1981) observed that dorsoventral width of
the condylar cartilage was more affected than
anteroposterior length by the absence of i n
utero muscular contractions of mutant mice
with muscular dysgenesis. This observation
suggests that condylar length may be under
less genetic control than are other condylar
dimensions. The presence of sexual dimorphism in human condylar width, but not length
(Wedel et al., 1978; Hinton and Carlson,
1979), also suggests that condylar width is
under more genetic control than length.
Evolutionary considerations
This study demonstrated that significant
morphological alterations of the craniofacial
complex can be manifested by lesions to motoneurons within the CNS. The secular modifications of the craniofacial complex during
the course of human and primate evolution
have been and continue to be well documented by numerous investigators (see
Moore and Lavelle, 1974 for a review). Hypotheses for explaining these morphological
changes have often entailed some change@
in masticatory function (HrdliEka, 1910;
Carlson and Van Gerven, 1977; Hylander,
1977, 1979; Cachel, 1979; Hinton and Carl-
son, 1979; Cartmill, 1980; Smith et al., 1983).
Data presented here and previously (Byrd,
1984) demonstrate that muscle activity patterns, masticatory function, CNS motoneuron systems, and craniofacial morphology are
all interrelated. All muscle-activity patterns
and functions influencing craniofacial morphology have a neurophysiological and neuroanatomical basis. In addition, different
taxa possess different neurophysiological
andor neuroanatomical mechanisms that effect their respective patterns of mastication
(Byrd, 1985).This concept can also be applied
to the muscles of facial expression. For example, Washburn (1946) repeated the facialnerve avulsion experiments he had performed on rats a second time on rabbits;
whereas the rats showed rostral deviation
away from the operated side (identical to data
presented here for FMNu lesioned rats), rabbits demonstrated rostral deviation toward
the operated side.
In recent years, many paleoneurology studies have concentrated on encephalization and
cerebral cortex changes during the course of
primate evolution (Falk, 1980). Data presented here, however, suggest that an appreciation of the roles played by pontine motor
nuclei (FMNu and TMNu) and by their manifestations as faciallmasticatory musculature
acting upon craniofacial form are also important for more fully understanding the evolution of primate craniofacial complexes.
I would like to thank the following people
for their support, comments, advice, and assistance during the course of this study: Drs.
Cedric Minkin, Michael Melnick, Tina Jaskoll, Messrs. Pablo Bringas and Val Santos,
and Martin Fong for his photographic
This research was supported by NIH grants
2 SO7 RRO5303-24, and 1R23 DE07380.
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motor, sequelae, nuclei, facial, lesions, craniofacial, trigeminal, growing, rats
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