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Unmyelinated axons in the feline trigeminal motor root.

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THE ANATOMICAL RECORD 214~198-203(1986)
Unmyelinated Axons in the Feline
Trigeminal Motor Root
M h T E N RISLING, KAJ FRIED, CLAES HILDEBRAND, AND ANNA CUKIERMAN
Department of Anatomy, Karolinska Institutet, Box 60400, S-104 01 Stockholm, Sweden
ABSTRACT
The trigeminal motor root was studied in the electron microscope
at different proximodistal levels in eight adult cats. Counts at a level halfway
between the trigeminal ganglion and the pontine junction showed that the root
contains about 9% (n = approximately 300) unmyelinated axon profiles at this level.
Small groups of unmyelinated axons occur on both sides of the PNS-CNS border, in
the surrounding pia mater, and in perivascular spaces of the CNS compartment.
Examination of serial sections from the PNS-CNS transitional region showed that
some unmyelinated axons actually cross the PNS-CNS border. The functional significance of these fibres remains unknown.
Both in the cat and in man spinal ventral roots contain
significant numbers of unmyelinated sensory axons,
many of which relay nociceptive information from peripheral receptive fields (see Coggeshall, 1980). It has
been proposed that ventral roots channel these axons
into the CNS, which would contradict the law of Magendie (see Coggeshall, 1980). As judged from recent electron microscopic (EM) studies of the PNS-CNS
transitional region, however, the law of Magendie is
valid (Risling et al., 1984). The EM results show that
the unmyelinated axons in the feline ventral root L7
either leave the root and project to the pia mater or loop
and course in a peripheral direction. Unmyelinated axons entering the spinal cord through this root have not
been found (Risling et al., 1984). The motor root of the
trigeminal nerve in the adult cat contains about 10%
unmyelinated axons and it has been suggested that it
might represent an additional pathway for trigeminal
pain (Young, 1978; Young and Stevens, 1979). The trigeminal motor root is only partly analogous to spinal ventral roots, since myelinated proprioceptive axons do
enter the CNS through this root (May and Horsley, 1910;
Pelletier et al., 1974; Ryu and Kawana, 1985).In view
of this principal difference between trigeminal and
spinal motor roots, the present study sets out to examine
whether unmyelinated axons cross the PNS-CNS border
of the trigeminal motor root.
MATERIALS AND METHODS
Material was taken from eight adult cats aged 1-6
years. The animals were anesthetized with sodium pentobarbital (Mebumal, 40 m g k g i.p.1, artificially ventilated, and perfused with Tyrode’s solution followed by a
solution of 5% glutaraldehyde and 0.1 M sucrose in a
300-mOsm phosphate buffer (Carlstedt, 1977a). After
perfusion each trigeminal ganglion was removed with
its motor and sensory roots attached to a piece of the
ventrolateral pons. After postfixation in glutaraldehyde
the motor root, including its junction with the pons and
portions of the most proximal part of the sensory root,
was carefully trimmed out. After buffer rinse, osmica0 1986 ALAN R. LISS. INC.
tion, and acetone dehydration the specimens were
embedded in Vestopal W (Carlstedt, 1977a). Semithin
toluidine blue-stained sections were used for orientation. Thin transverse sections covering the whole motor
root were cut a t the following levels: 1)the proximal end
of the trigeminal ganglion, 2) approximately halfway
between the ganglion and the pons, and 3) the proximal
end of the motor root close to the pontine junction. At
the latter level the sections included the PNS-CNS transitional region of the sensory root. In addition, a series
composed of 1,517 consecutive thin transverse sections
were cut from the PNS-CNS transitional region of the
motor root. The sections were collected on one-hole copper grids coated with carbon-stabilized Formvar, contrasted with uranyl acetate and lead citrate, and
examined in a Philips EM 301 electron microscope.
RESULTS
In the electron microscope the motor root fascicles
were easily identified and differentiated from the sensory root and from the small accessory sensory fascicles
on the basis of the markedly different fibre size distributions (Fig. 1) (Young, 1977). At the distal level the
motor root formed a rather coherent bundle composed of
large and medium-sized myelinated axons and a n occasional neuronal perikaryon. Unmyelinated axons also
occurred among the myelinated axons and these were
sometimes arranged in large bundles. At the middle
level neuronal perikarya were not observed and the
bundles of unmyelinated axons tended to be smaller but
more numerous. At this level approximately 9% of all
axon profiles were unmyelinated (range 6.8-11.0%, n =
3). The total number of unmyelinated axon profiles per
motor root varied between 231 and 305. At proximal
levels, which included the glial fringe (Berthold and
Carlstedt, 19771, unmyelinated axons surrounded by astrocytic processes formed islands between myelinated
PNS-type axons, with or without the participation of
Schwann cell-like profiles (Fig. 2a,b). On the CNS side
Received March 1, 1985; accepted September 10, 1985.
199
TRIGEMINAL MOTOR ROOT
Fig. 1. Low-power electron micrograph showing a transverse section
from a fairly proximal level of the trigeminal root region. The picture
shows fascicles of the motor root (M) partly surrounding the larger
sensory root (S).At this level the motor root fascicles remain in the
PNS compartment, while the sensory root contains a large core of CNS
tissue. Note the relatively high proportion of large myelinated axons
in the motor root fascicles compared to the sensory root. x 160.
of the PNS-CNS transition a few small groups of unmyelinated axons were observed. At places close to the
surface of the CNS these axons were sometimes approached by slender fibrous astrocytic processes and
patches of a n electron-dense axolemmal undercoating
could be present at such sites (Fig. 2c). In addition, a few
small myelinated axons could be observed superficially
in the CNS compartment. Occasional small groups of
unmyelinated axons were also encountered at deeper
levels in the CNS compartment (Fig. 2d). It was not
possible to count unmyelinated and small myelinated
axons at deeper CNS levels, because the motor root
fibres were not clearly demarcated from those of the
sensory root (Ryu and Kawana, 1985). The total number
of CNS-type axons with diameters below 1 pm was,
however, estimated to be less than 100.
The results from the series composed of consecutive
sections have been illustrated in Figures 3 and 4.Figure
3 shows a bundle of unmyelinated axons which could be
followed from the PNS compartment of the motor root
into the CNS. The axon shown in Figure 4 was myelinated both in the PNS and the CNS but possessed a n
about 20 pm long unmyelinated segment a t the PNSCNS transition.
Larger blood vessels within the CNS compartment
were often accompanied by one to three perivascular
nerve bundles, each of which contained some five to
thirty unmyelinated PNS-type axons (Fig. 5a). Finally,
the pia mater in the vicinity of the PNS-CNS transition
of the trigeminal motor root contained tiny bundles of
unmyelinated and small myelinated PNS-type axons
(Fig. 5b).
DISCUSSION
The present results confirm previous evidence that the
main trunk of the feline trigeminal motor root contains
approximately 10% unmyelinated axon profiles (Young
and Stevens, 1979). It has been suggested that these
axons are sensory (Young and Kruger, 1981). Our results
show that unmyelinated axons are present on both sides
of the PNS-CNS transition and at deeper levels in the
CNS compartment of the motor root. At least some of
these unmyelinated axons actually cross the PNS-CNS
border. Larger unmyelinated PNS axons tend to become
myelinated as they enter the CNS (Carlstedt, 1977b).
Therefore the few myelinated axons with diameters below 1pm which occurred superficially in the CNS compartment, might be unmyelinated on the PNS side of
the transition. These findings show that, in contrast to
the ventral root L7 (Risling et al., 1984), the trigeminal
motor root represents a site where some unmyelinated
200
M. RISLING, K. FRIED, C. HILDEBRAND, AND A. CUKIERMAN
Fig. 2. Electron micrographs from transverse sections through the
PNS-CNS transitional region in the trigeminal motor root of an adult
cat. a) Two profiles resembling unmyelinated axons (*) are associated
with both astrocytic processes of the glial fringe and with Schwann
cell profiles. ~ 3 5 , 0 0 0b)
. This field shows several unmyelinated axons
(arrows) and a small myelinated axon in an island composed of CNS
tissue (astrocytic processes). Note the surrounding PNS-type large
myelinated axons. x 14,000. c) The three unmyelinated axons indicated
by asterisks occupy superficial positions in the CNS compartment of
the motor root at the level of the pontine surface. The myelinated axon
also present is located on the PNS-side of the transition. One of the
axons (right) is partly apposed by radially oriented astrocytic processes
and exhibits an electron-dense axolemmal undercoating at these sites
(arrowheads). ~ 2 4 , 0 0 0d)
. This picture illustrates a group of unmyelinated axons (*) at a deeper level in the CNS compartment of the motor
root. Note the surrounding astrocytic processes and the CNS-type
myelinated axons (top and left) nearby. ~ 2 5 , 0 0 0 .
TRIGEMINAL MOTOR ROOT
Fig. 3. Electron micrographs from the series of transverse sections
through the PNS-CNS transition of the trigeminal motor root. Distally
(a = section number 750) a group of unmyelinated axons (arrows) is
associated with a Schwann cell in the PNS compartment. More proximally (b = section number 1,151) the group of axons has split into
three small clusters of unmyelinated axons (arrows), which are found
immediately beneath the surface of the CNS compartment. The last
201
micrograph (c = section number 1,181)shows the same clusters at a
deeper position within the CNS compartment. At this proximal level
the unmyelinated axons are completely surrounded by astrocytic processes. The long arrow indicates a comparatively large unmyelinated
axon in which an patchlike electron-dense axolemmal undercoating
was observed at some levels. This axon, however, remained unmyelinated throughout the series. x 12,000.
202
M. RISLING, K. FRIED, C. HILDEBRAND, AND A. CUKIERMAN
and small myelinated axons shift from the PNS to the
CNS or vice versa.
The presence of unmyelinated axons in the trigeminal
motor root and on both side of the PNS-CNS transition
may be explained in various ways: 1)It is known that
serotoninergic brainstem neurons project to pial blood
vessels (Chan-Palay, 1976; Edvinsson et al., 1983) and
some of these axons might travel to their leptomeningeal targets through cranial nerve roots. Thus, some
proportion of the unmyelinated axons in the trigeminal
motor root might represent efferent axons from brainstem neurons. 2) Adrenergic, cholinergic, and peptidergic fibres are related to the adventitial surfaces of
large cerebral pial arteries (Edvinsson, 1982).The proximal segments of these arteries are among the few intracranial structures which, when stimulated, elicit the
sensation of pain (Mayberg et al., 1984). The trigeminal
ganglia seem to represent the most important source of
afferents from pial blood vessels (Kautzky and Wolter,
1952; Mayberg et al., 1984). By analogy with unmyelinated ventral root axons, some of the unmyelinated axons
in the trigeminal motor root might then leave this root
and enter the pia mater (Risling et al., 1984). Accordingly, unmyelinated and small myelinated axons unrelated to blood vessels were seen in the pia mater
surrounding the pontine entrance of the motor root. 3)
Unmyelinated sensory axons might form loops in the
motor root in the manner described for cat ventral roots
misling et al., 1984). 4) Finally, unmyelinated axons in
the trigeminal motor root might, to some extent, represent sensory axons, which enter the CNS together with
the large-caliber proprioceptive afferents known to be
present (May and Horsley, 1910; Pelletier et al., 1974).
The involved fibers are so few, however, that they are
not likely to represent a pathway of any major significance for trigeminal nociception.
ACKNOWLEDGMENTS
This study was supported by grants from the Swedish
Medical Research Council (project 37611, the Karolinska
Institute, the Swedish Society of Medicine, Magn.
Bergvalls stiftelse, and A ke Wibergs stiftelse. We wish
to thank Ms. Pippi Lindqvist and Ms. Maria Meier for
excellent technical assistance.
~
Fig. 4. Electron micrographs from the series of transverse sections
through the PNS-CNS transition of the trigeminal motor root. Figure
4a (section 750) shows a small myelinated axon (*) on the peripheral
side of the PNS-CNS border. Note the neighboring astrocytic processes
of the glial fringe. More proximally (b = section 867), the axon (*) is
surrounded by an inner Schwann cell layer and an outer astrocytic
layer and it has lost its myelin sheath. Figure 4c (section 1,211)shows
the same axon (*) in a superficial flap of the CNS. Also at this level
the axon is unmyelinated. In the last micrograph (d = section 1,347)
the axon (*) is surrounded by a CNS-type myelin sheath and is located
deeply within the CNS compartment of the motor root. X 17,000.
TRIGEMINAL MOTOR ROOT
203
Fig. 5. Electron micrographs from transverse sections through the
trigeminal motor root at a level near the pons. a) This bundle of PNStype unmyelinated axons (arrow)is located in the adventitia of a larger
blood vessel CL = lumen) within the CNS compartment of the motor
root. ~ 6 , 0 0 0b)
. This field shows a group of PNS-type unmyelinated
axons (arrow) and one small myelinated axon within the pia mater
PIN unrelated to blood vessels. The pontine surface can be seen in
the lower part of the picture. ~ 3 , 0 0 0 .
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