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Occurrence of neurons in the sciatic nerves of albino rats.

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OCICTJRBENCE O F NEITRONS I N THE SCIATIC
N E R V E S O F ALBINO R A T S
SEVEN FIGIJKES
A consideration of the location of iieuihoiis usually leads
to the classic areas described in most ariatorriical textbooks,
that is, the central nervous system, the cranial, spinal and
autonomic ganglia. However, it is ell established that aherm i i t neurons do occur; primarily in two areas, the cranial
nerves and in ventral and cloi*sal spinal roots.
Investigation of tlic cranial iierves in areas other than the
narrietl ganglia by several woiakers has rc~vealeclthe location
of neurons in cranial iiervcs TTI, V, VI, I X , X, X I and XII.
Nicholson ('24) reported iieurons of the sensory type on the
oculoniotoi. and abtlucens nerves iiisitlc tlie orhital cavity in a
liurriari fctus. Peters ( 7%) repoi*ted sensory typc neurons,
central to the semilunar ganglion on tlie trigeminal nerve i n
thcl cat, ox, guinea pig and man. Falimy ( '2.7) dcscrilml Ilipolar-like neuroiis on the extracranial parts of thc glossopharyngeal, vagus aiitl spinal ace ory iierves of man, while
sensory type neurons on
Tarkhov and El-Malek ('r>O) fou
peripheral portions of the hypoglossal nerve iii dogs, cats,
rats, rabbits and man.
T l i ~occurreiicc of tiherrant iic'ui'ons i n the spiiial roots is
also well clocurrientetl. Duiican arid Crockw ( '39) found such
cells to lie particularly iiumerous on the dorsal roots in the
dog. Ohscrvations of tlic ventral spinal roots of cats ant1 of
Prrsrnt adilress: Drpnrtincnt of Aiintoniy,
Mciliciiic., C0r:il G:il)lrs, Florit1:i.
I9i
T'iii
it? of 3li:imi School of
19s
METZ, J U D I C E AND FINERTY
a hunian fetus by Windle ( '31) revealed sensory type neurons
scattered throughout these roots. Gaugliou cells of the autonomic type have also been described in nlan on the rami
cornmunicantes of the spinal nerves by Skoog ( '47). Excellent
historical reviews of tllese subjects may be found in the ITports by Peters ( '35)' Windle ( '31) arid Skoog ('47).
The present study deals with the occuimmce of alwrraii t
ganglion cells in a previously undescribed site, the sciatic
nerve. During histological observation of rate of regeiieration
of sciatic nerves anastoniosed between parabionts, neurons
were noted in various locations on the nerve (Metz and
Fincrty, '54). The present report describcs the morphology
and location of these nerve cells on the sciatic ilprve uric\ its
branches in albino rats.
M A T E R I A I S AND METHODS
( h u p I consisted of 15 sciatic nerves from adult Holtzrnan
rats in which the nerves had been severed and sutured to
allow regeneration ( 9 between parabionts and 6 in single r a t s ) .
These were nerves taken from the previously-puhlishd study
( AIetz and Finerty, '54).
Group 11 consisted of 31 sciatic nerves from adult normal
Holtzman rats.
Group 111 consisted of sciatic nerves of immature Holtzman
rats, removed as follows: one at birth, 4 at one week of age,
two at two weeks, one at three weeks and two a t 5 weeks.
Group I B included two sciatic nerves which had heen severed and allowed t o degenerate for 30 days prior to removal.
The procedure for removing the nerves consisted of sacrificing the animals arid exposing the sciatic nerve and its branclies.
The nerve was severed proximally in rclation to the great
trochanter of the femur and distally at a point where the main
branches of the nerve (the anterior tibia1 arid comrrion peroncal) enter the muscle mass of the leg. The nerves were theii
placed in a suitable fixative, imbedded and sectioned s c ~ i a l l y
in a longitudinal plane a t either 10 or 15 1-1 in thickness.
N E U R O N S I N T H E SCIATIC NEHVE
199
Foi. ease of location of neuroiis Nissl stains were used
on the niajority of the nerves studied. The two Nissl stains
which were most suitable were a buffered thionine stain and
the cresyl echt violet stain, both of which gave satisfactory
results. I n order to identify neuron processes a modified
Protargo1 method and a modified pyridine silver method were
uscd. The nerves in the fourth group were stained by a 1%
solution of osmium tctroxide. I n addition to the above stains,
Hematoxylin and Eosin, Heidenhain’s Iron Heniatoxylin ancl
hfallory’s Triple stain wei-e used on a few slides.
I n recording the number of cells found in microscopic
examination, the cells were counted only if a nucleolus was
present. I n a few cases where actual ganglia existed, the
cells were so closely packed that an estimate of the total
number of cells present was made, rather than an actual
count.
Tn addition to the sectioned material, hulk staining was
attempted with some success on 1 2 of the nerves of Group IT.
The procedure consisted of fixation of the nerve in formolsaline and then staining in a solution of cresyl echt violet for
30 minutes to an hour. The stained nerve was differentiated
in 95% alcohol, and then carried through dehydration by
three changes of absolute ethyl alcohol and finally cleared in
xylol. The nerves were examined under a low power binocular
dissecting scope (12 x oculars and 3 x objective) noting the
location of the ganglia. The ganglia \\”re then manually
teased apart from the neive and permanently rnountetl on a
s1i d e.
RESULTS
Histological examination of‘ the sciatic nerve revealed the
presence of neurons in 51 of the 58 rat nerves studied (figs.
l,2) . Similar numbers and locations were found in all of the
adult nerves studied with no differences noted as a result of
regeneration. The numbers of neurons observed ranged from
1 to 144 cells per nerve. I n the immature normal r a t s of
Group I11 variation was more limited, the number of neurons
ranging from 4 to 55 cells per nerve. Microscopic study of
200
METZ, J U D I C E ANL) F l N E I t T Y
the sectioned degenerated nerves of Group IV revealed the
presence of 9 ganglion cells iii oiie nerve and 150 in the other,
even though no intact niyelin sheaths could be seen.
The neurons were found in t h i w typical locations in a
cross sectional aspect of the sciatic nerve. The first of these
positions corisistcd of small groups of iieurons 1 to 10 in
number, usually found ill the ceiitcr of the bundles of nerve
fibers composing the iicrve. The long axes of such gaiiglioii
cells were parallel to the long axes of the nerve fibers. The
secoiid position was the occurrence of slightly larger gi’oups
of neurons, 5 to 15 iii tiurril)er, located between the bundles of
i ~ e r v efibers and their peiiucuriurn. A third group of neurons,
25 to 50 iii nurril)ei-, occasionally appeared on one of tlic
smaller braiiches of (4tliei. the commoii peroiieal or t ibial
divisions (fig. 3 ) . The iieuroiis in these srnaller 1)i~iiiclies
were closely packed tlii+ougliout the mitire tliarrietei. of the
nerve, often produciiig a local ciilargcniciit. Seiu*ons w e i ~
most commonly fourid in the first two positions noted above.
The locatioii of neui’oiis i i i a longitutliiial plane ill the sciatic.
iiervo varied from nerve to i i ( ~ i * wA
. siiigle nerve often sho\\-rtl
three, 4 0 1 - more diffcwiit groups of cells scattered along its
lengtli. Tlieir position occurred allywhere from the first cutaiicous hranch of the tibia1 divisioii, i n the regioii of the greatcr
ti.ochaiitei*of tlie fernur, to the ciit ranee of the conimon pci’oncal aiid tikial nerves into tlic muscle mass of the leg. Tlic
largest i i u n i l ~ rof neurons, a i d particularly the large clust(lrs,
appeared to he located on the main branches of the sciatic
nerve, i.e. tlie comnioii pei*oiical anti tibia1 nerves. Tliesc two
iicrves share a conimon iiei’vc sheath (cpineui*iuni) to a point
midivay in the thigh aiid it is distal to this point that thc
majority of the ganglion cells occuix Studies with d i o l ~
mounts coiifirm these locations.
Cell morphology, as studied in Nissl stain prcl)arntions ant1
silver preparations, showed tlie ganglion cells to be eitlici.
oval (fig. 1) o r spherical (fig. 2) in shape. The oval 01elongated ganglion cells, such as those appearing in the center
of the nerve bundles, had diameters of 15 to 20 a r i d 1~1igtlls
of 33 to 53 p. Other rieuroiis, particularly those in the large.
ganglia tended to be more splicrical with diameters of approximately 25 to 35 p. The nuclei of the ganglion cells were
large, clear, oval in shape aiid w e i ~ccntrally located (figs. 4
aiicl 5). They were characte~.izedby a fine chromatin network
and a prominent iiucleolus, usually eccentrically located. The
cytoplasm contained srnall granular clumps of Sissl material
scattered diffusely throughout the cell body. The processes
were difficult to visualize. Some silver preparations (figs.
6, 7) showed processes of a unipolar nature similar to those
seen in sensory type neurons. Another, however, showed a
single neuron with several processes. Encapsulation by small
cells (figs. 4, 5) siniilar to those found in the spinal ganglia
was a characteristic feature of most neurons.
nrscussroK
The preseiice of ganglion cells in N peripheral soiriatic
nei-ve a s described in this investigation leads to a great deal
of speculation a s to their type, origin and function. A tliscussion of the type of neurons found is complicated because of
the morphological similarities between sensory ganglion cells
aiid those of the autonomic nervous system. The morphological features of the neurons studied would indicate that
they a r e of the sensory type. They are spherical to oval in
shape, have a cellular capsule of “satellite” cells and in one
silver preparation processes of the unipolar type were demonstrable. While these features a r e not coiiclusive evidence,
they certainly lend support to the idea that a portion of the
neurons studied a r e of the sensory type. The identification
of one multipolar iieuron does indicate, however, that more
than one neuron type may be present.
I11 this discussion the functional interpretation of the ganglion cells can be based only on morphological characteristics,
and a s described the unipolar type might possibly serve the
role of a sensory ganglion cell transmitting afferent impulses.
The niultipolared cell may function as an autonomic coniponent acting as a terminal ganglion. Determiiiktion of the
actual fulictioii of thcsc iicuroiis will depeiid oii ncuro-l)liysiological study.
The origin of these neurons, in tlic scope of this discussion,
is of necessity a matter of conjecture. If the iieuroiis are of
a sensory type as discussed it is probable that the cells have
their o~*igiiiin the doi*sal root ganglia or their soui*cc, thcl
1icu1dcrest, although it is not possible to exclude other parts
of tlic enibryoiiic iiei’vous s y s t c m . Pei-haps duriiig tlie migration of the neural crest to its position a s the tloiwll root
ganglia, cellulai. elenleiits map have migrated to a more distal
point than usual. TTitli the coiitiiiued growth of tlic spinal
iicrvcs and the niigratioii of the muscle masses associated
with tlieni these iieurons niay have heeii carried to tlie peripheral positioii they iiow occupy. This type of niigratioii
~vouldalso be applicable to sourc
other than the ncural
c rc s t .
Tlic extreme variation in the number of iieurons p(li* iierve
in the sciatic nerve of the normal animals of Group I1 nialics
it impossible to evaluate tlie significance of their number.
This variatioii could lie clue either to an actual differelm i n
tlie iiumher of iicui*oiis or due to errors inherent iii the
counting pimedurc. Every effort was made to locate ant1
count all of the ganglion cells present within a given ~i(si-vc.
The possibility remains that even with very careful tcchiiiquc
sonic of the neurons map not have beeii fouiid 01’ that in tho
larger ganglia a n inaccurate approximation of the numl)e~of iiourons was made. Even though the first observation of
these cells was made in regencrated nerves of pal-abiotic rats
it now is apparent that the pi~evioustrciatmeiit had 110 i.clIatioii
to the presence of these neurons.
Thcl question as to whether these iieurons are a characteristic of rats is unanswei*ed a s yet. Examination of four mOUse
sciatic nerves failed to reveal any, hut further study of incideiice of these aberrant cells i n other species and in other
peripheral nerves rcniains to he clone.
NEURONS I N THE SCIATIC NERVE
203
SITMMARY
Fifty-eight sciatic nerves of albino rats were studied hy
various histological techniques. Neurons were found in 51
of the 58 nerves studied, both unipolar arid multipolar types.
The number of neurons per nerve varied from 1 to 144. They
were found at several different sites along the length of the
nerve examined, with the largest number occurring at the
bifurcation of the sciatic nerve into its two main branches. A
technique for the bulk staining of nerves using Cresyl echt
Violet is described.
L I T E R A T U R E CITED
D., A N D E. 8. C'ROCKER 1939 Aberrant ganglion cells as a ~ O U I ' C C of
intact fibers in scvered dorsal roots. J. Neurophysiol., 2 : 3-8.
1927 A note on the intracranial and extracranial parts of thc
FaHhru, S. A.
I X t h , Xth and XIth nerves. J. Anat., 6 1 : 298-301.
1954 Functional nerve regeneration between p a r a
METZ,G., AND J. C. FINERTY
biotic rats. Anat. Rec., 228: 442.
XICHOLSOPI',
H. 1924 On the presence of ganglion cells in the third a n d sixth
nerves of man. J. Comp. Neurol., 37 : 31-36.
PETERS,
G. A. 1935 The presence of sensory nerve cells in the central root of
the trigeminsl nerve. J. Comp. Neurol., 62: 349-360.
HICOOG, T. 1947 Ganglia in the communicating rami of thc cervical sympathetic
trunk. Lancet, 8: 4 5 7 4 6 0 .
T A R K H ~A
N., A., AND S. ABD. EL-MALEK 1950 On the presence of seiisory iierrc
cells on the hypoglossal nerve. J. Comp. Neurol., 9 3 : 219-228.
WINDLE,W. F. 1931 Neurons of the sensory type in the ventral roots of ma11
and other mammals. Arch. Neurol. and Psych., 2 6 : 791-800.
L)UKCIK,
1 Microaopic section of the sciatic iwrvc dmwing w ganglion cell. Crcsyl ccht riolct;
X 1139.
3
A ganglion that fitis been aitiiiutill~tctiaed q w t froin
sciatic nerve. Cresyl eeht violet; X 340.
$1
~rliolr.uioiiiit i)rrprirtitioii of tlw
3 Microscopic section of a large gaiigliou appearing 011 a eiiiall braiieh of the sciatic iiervp.
Cresyl echt. violet; X 170.
4 1\~Iicroscopic,section of the sciatic nerve showing gaiiglioii cdls. JIodified protargol silrcistain; X 731.
Microscopic section of the sciatic nerve showiiig gaiiglion cclls. Modified protnrgol si1vc.r
stain; X 340.
G Microscopic section of the scixtic iierrc showing gaiiglioii cc4ls a i i d processes. JIodified
pyridine silver stain; X 731.
7 Microscopic section of the sciatic IICI'VC sliowiny ganglion cells mid processes. Modifird
pyridine silvcr stain; X 731.
5
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