opdam et al-1976-journal of comparative neurology
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Topological Analysis of the Brain Stem of the Axolotl
mbystoma mexicanum
P A U L O P D A M AND R U D O L F
NIEUWENHUYS
D e p t i r t r n e n t
of
A n i i t o m y , U n w r r s i t y
of
N i j m r . g t , n ,
N i j m e g z n ,
The
N r t h e r l t r n d s
ABS T RACT The ventricular sulcal pattern and the cellular structure of the
brain stem of the axolotl
A m b y s t o m a mexicanum
have been studied in trans-
versely cut Nissl and Bodian stained serial sections. Six longitudinal sulci,
the sulcus medianus inferior, the sulcus intermedius ventralis, the sulcus
limitans, the sulcus intermedius dorsalis, the sulcus medianus superior and the
sulcus lateralis mesencephali could be distinguished. A seventh groove, the
sulcus isthmi, clearly deviates from the overall longitudinal pa ttern of th e other
sulci. Although most neuronal perikarya are contained within a diffuse peri-
ventricular gray,
19
cell masses could be delineated; seven of these a re primary
efferent or motor nuclei, four are primary afferent or sensory centers, four
nuclei are considered a s components of the reticular formation, and the remain-
ing four cell masses ca n be interpreted as “relay” nuclei.
In order
to
study the zonal pattern of the brain stem, this structure was sub-
jected to a topological analysis cf Nieuwenhuys,
’74
an d fig. 13). This analysis
yielded the following results. In the rhombencephalon the grisea are arranged
i n four longitu dinal zones whic h, following Kuhlenbeck, have been termed:
area ventralis, area intermedioventralis, area intermediodorsalis and area
dorsalis. Where present the sulcus intermedius ventralis, the sulcus limitans
and the sulcus intermedius dorsalis mark the boundaries between these four
morphological entities. The zonal areas in question coincide largely, but not
entirely, with the so-called functional columns of Herrick a nd Johnston. Th e
most obvious incongruity is th at the ar ea intermediodorsalis contains, in addi-
tion to the nucleus fasciculi solitarii and the nucleus visceralis secundarius,
two
non-visceral sensory cell masses, namely the nucleus vestibularis magno-
cellularis a nd the nucle us cerebelli. The four morphological zones delineated
in the rhombencephalon cannot be distinguished in the mesencephalon and it
is of particular importance th at th e sulcus limi tans does not extend into this
part of th e brain . Functionally, however, the medial part of the tegmentum
mesencephali may be considered the rostra1 extreme of the somatic motor
column, whereas the tectum primarily represents a somatic sensory correla-
tion area.
The investigations of Gaskell (1886,
1889), His (1888), Herrick (1899), Johnston
(‘01) and many others have led to the
doctrine that the brain stem fundamen-
tally consists of a number of longitudinally
arranged
zones
or columns, some of which
are delimited from each other by distinct
ventricular sulci. In order to test the
validity of this columnar model for the var-
ious groups of vertebrates, one of us (Nieu-
wenhuys, ’72, ’74) has developed a proce-
dure which makes it possible to survey the
entire ventricular surface, with its sulci
J.
COMP.
NEUR.,65 : 285306
and the underlying cell masses, in a sin-
gle graphical reconstruction. Because in
this procedure the elementary principles
of
the branch of mathematics known as
topology are applied it has been termed
topological analysis. Such topological anal-
yses have been carried out already on the
brain stems of the lamprey
L a m p e t r a
flu-
via t i l i s (Nieuwenhuys, ’72) and of the tur-
tle
Tes t u do h erman n i
(Cruce and Nieu-
wenhuys, ’74). In the present paper the
results of a similar analysis of the brain
stem
of
the axolotl
A m b y s t o m a m e x i c a n u m
285
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286
PAUL OPDAM AND RUDOLF NIEUWENHUYS
will be presented. This study forms part
of the program of research outlined in a
previous publication (Nieuwenhuys, '74).
A review of the extensive literature on
the brain stem of tailed amphibians will
not
be
attempted. It may be stated here,
however, that the fundamental studies of
C. J. Herrick ('14, '17, '30, '48) have been
invaluable sources
of
information through-
out the whole investigation.
MATERIAL AND TECHNIQUES
Young specimens of Ambystoma m e x i -
canum, measuring 15-20 cm, were em-
ployed in the present study. The animals
were anaesthetized in a 0.025% solution
of M.S. 222 (Sandoz), and perfused through
the heart with Heidenhain's SUSA mix-
ture or with Formalin-Aceto-Alcohol. The
brains were removed, embedded in paraf-
fin, cut transversely at a thickness of 20 pm
and stained with cresylecht violet or with
silver proteinate according to Bodian. For
the study of the glial pattern we em-
ployed the brains of two specimens pre-
pared by the rapid Golgi technique. These
brains were embedded in celloidin and
sectioned at 80 pm.
PROCEDURE
The reconstruction represented in fig-
ure
13
was based on a continuous Bodian
series. Drawings of some 50 equidistant
sections of this series were made with the
aid of a projection apparatus at a mag-
nification of 100 diameters. The cell pic-
ture was studied at higher power with the
microscope and the cell masses were de-
lineated on the drawings. In these draw-
ings the ependymal and meningeal sur-
faces were connected by a number of
curves, termed projection curves. These
curves were derived from the main stream
of the glial fibers, as observed in our Golgi
preparations. These Golgi preparations re-
vealed that throughout the brain stem the
ependymal gliocytes are provided with long
basal processes, which span the entire
width of the wall. Although these proc-
esses show profuse ramification, an overall,
radial pattern can be readily recognized.
It is with the aid of these radially orie-
ented projection curves that the outlines
of the cell masses, situated at various
depths in the brain stem wall, are pro-
jected upon the ventricular surface. In
each drawing the deepest point of the ven-
tricular mid-line groove of the brain stem
is defined as the zero point. With the aid
of a curvimeter, the distances from the
zero
point to the deepest point of other
sulci and to the projections of the outlines
of the nuclei upon the ventricular surface
are determined on both sides.
All the dis-
tances are measured along the ventricular
surface and plotted graphically on a line.
In the final reconstruction all such lines,
derived from the individual sections are
placed in their correct rostrocaudal se-
quence, spaced appropriately, with their
zero points connected by a single longi-
tudinal line, which forms the midline of
the reconstruction. Finally, best fitting
curves are drawn through the sets of points
belonging to one and the same structure
(for a more detailed description and a crit-
ical evaluation of the topological recon-
struction procedure the reader is referred
to Nieuwenhuys, '74).
In the reconstruction (fig. 13) the levels
of the drawings on which it is based are
indicated on both sides by short horizontal
lines. Ten sections were selected to pro-
vide an atlas of the brain stem of
the
axolotl. They are represented in the fig-
ures 2-11; their levels are indicated in
figures
1
and
13.
In order to gain an insight into the size
of the cells in the various nuclei, ten
cells of each cell group were drawn at a
magnification of 500 diameters, using a
Zeiss drawing prism. In these drawings
the size
of
the somata was determined
by
averaging their diameters measured
in
two
directions perpendicular to each other.
When a particular griseum appeared to
contain more than one cell type, ten ele-
ments of each type were sampled and mea-
sured. The arithmetical average of the
data obtained from the ten individual cells
of each type is indicated in the descrip-
tion of all nuclei.
The cells in the brain stem of the axo-
lotl show considerable differences in size,
ranging from 1 1 4 2 pm, the Mauthner
cells not included. For convenience of de-
scription we have subdivided the cells into
three categories: small cells, measuring
11-15 pm, medium-sized cells, measuring
1 6 3 4 pm, and large cells, measuring
3 5 4 2 p m.
In order to explore the distribution and
density of the larger cells of the reticular
formation the following procedure was fol-
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B R A I N STEM
OF A M B Y S 7 O M A
287
lowed. All conspicuous neuronal elements
within this field were measured and those
larger than 19 pm were plotted on a
preliminary version of the topological map.
By
introducing a second threshold at
35
pm
this group was subdivided into intermedi-
ate and large reticular elements. In the
final version of the map (fig. 13) only one
out of three cells of each category is rep-
resented for purposes of clarity.
The large elements constituting the nu-
cleus mesencephalicus of the trigeminal
nerve have also been charted in the map.
G ross f e a ture s
The brain stem as defined here includes
the rhombencephalon and the mesenceph-
alon (fig. 1). The rhombencephalon is rela-
tively very large. It includes bilaterally a
horizontal basal plate and, throughout
most of its extent, a vertically oriented
alar plate. The most rostral part of the
rhombencephalic alar plate arches around
a lateral recess of the fourth ventricle and
continues into a transversely oriented band
of tissue, which fuses in the median plane
with its counterpart of the opposite side.
The nervous tissue which constitutes the
rostrolateral wall and the rostral part of
the bottom of the lateral recess represents
the auricula cerebelli. The corpus cerebelli
is constituted by the fused, transversely
oriented bands of tissue. The latter form
a small cap over the most rostral part of
the fourth ventricle. The remaining part
of this ventricle is covered by a choroid
roof which is attached to the dorsal aspect
of the alar plates and to the caudal edge
of the cerebellum. The tapered, most
ros-
tral part of the rhombencephalon, is known
as the isthmus rhombencephali.
The mesencephalon is small and has
essentially maintained the early embryonic
tube-like condition of the brain. Its ver-
tically oriented, cleft-like ventricular cav-
ity
is dorsally surrounded by the tectum
and ventrally by the tegmentum mesen-
cephali. The boundary between these two
regions is not indicated by any externally
visible landmark. Caudally the tegmentum
mesencephali is directly continuous with
the rhombencephalic basal plate. The tec-
tum passes, v i a a short velum medullare
anterius, into the corpus cerebelli.
Due to its extremely simple configura-
tional relations, almost the entire ventric-
RESULTS AND COMMENTS
ular surface of the brain stem of the axolotl
could be mapped out, as shown in figure
13. Only the caudal portion of the corpus
cerebelli and the larger part of the auric-
ulae had to be omitted from this recon-
struction.
Ven tr icular sulc i
Since, according to several authors (RO-
thig, '27; Kuhlenbeck, '27; Gerlach,
'33,
'46)
the ventricular sulci represent highly
important morphological landmarks, the
course and extent of these structures has
been carefully analysed in the present
study.
The
s u l cu s m e d i a n u s i n fe r io r
is well de-
fined throughout almost the entire brain
stem, although it varies in depth and width.
In the caudal part of the midbrain and
in the isthmus region this sulcus widens
and forms a narrow depression (figs.
9,
lo) . It is lacking in the most rostral part
of the midbrain since here the mesence-
phalic floor arches, v ia the tuberculum
posterius, over into the membranous roof
of the hypothalamus. Hence, the lateral
walls of the rostral mesencephalon are
not only rostrally, but also ventrally di-
rectly continuous with the walls of the
diencephalon
c f .
Herrick,
'35:
fig.
1).
The
sulcus medianus inferior, which delineates
the raphe at the ventricular side, is of
paramount importance in the present study
because i t constitutes the axis of the top-
ological reconstruction (fig. 13). It should
be noted that in this reconstruction the
walls of the most rostral parts of the
mesencephalon have been mapped as if the
sulcus medianus inferior extends into this
region.
A sulcus in termedius ventral i s
is pres-
ent in the most caudal part of the rhomb-
encephalon. Rothig ('27) described for
Cry p tobranc hu s j ap on ic us
and
Siren lacer-
t ina a probable equivalent of this groove
under the name sulcus paramedianus ven-
tralis; according to this author the sulcus
separates the somatic motor area from
the visceral motor area.
The s u l c u s l i m i t a n s , which is generally
regarded as a landmark, indicating the
boundary between the motor basal plate
and the sensory alar plate, is indistinct.
In most places i t is merely represented by
a slight depression in the ventricular sur-
face (figs.
6). A t
the level of the Mauth-
ner cell the sulcus limitans fades out com-
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288
PAUL OPDAM AND RUDOLF NIEUWENHUYS
Abbr?.vitrtio?zs
a lin lat, Area lineae lateralis
auric, Auricula cerebelli
Cer, Nucleus cerebelli
corp cereb, Corpora cerebelli
dienc, Diencephalon
fsol, Fasciculus solitarius
Gran, Stra tum gran ulare cerebelli
Ipa, Nucleus interpedu ncularis pars anterior
Ipp, Nucleus interped uncu laris pars posterior
Is,
Nucleus isthm i
Mth, Mau thne r cell
N dors, Nucleus dorsalis areae octavolateralis
Nflm, Nucleus of the fasciculu s longitud inalis
N interm , N ucleus intermedius areae
n lat ant , Nervus lateralis anterior
n
lat post, Nervus lateralis posterior
n spin 2, Nervus spinalis 2
n
I
nervus olfactorius
n
111,
Nervus oculomotorius
n
V
Nervus trigeminus
n
V I
Nervus abduce ns
n VIIm, Nervus facialis ram us motorius
n VIII, Nervus octavus
n IX, N ervus glosso pharyn geus
n IXm, Nervus glossopharyngeus ram us
medialis
octavolateralis
motorius
n
I X s ,
Nervus glossopharyngeus ram us
sensorius
n X , Nervus vagus
Ra, Nucleus raph es
Ri, Nucleu s reticularis inferior
Rm, Nucleus reticularis medius
sa, Sulcus “a”
sid, Sulcus inter med ius dorsalis
sis, S ulcus isthm i
siv, Sulcus inter med ius ventralis
slH, Sulcus limitans of His
slm, Sulcus lateralis mesencephali
smi, Sulcus med ianus inferior
sms, Sulcus medi anus superior
Sp(in) mot col, Spin al motor column
tect, Tectum mesencephali
telenc, Telencephalon
Vem, Nucleus vestibularis magnocellularis
Visc, Nucleus visceralis secund arius
111,
Nucleus nervi oculomotorii
IV, Nucleus nervi trochlearis
Vm, Nucleus motorius nervi trigemini
Vme. Nucleus mesencephalicus nervi
VI, N ucleus nervi abducen tis
VIIm, Nucleus motorius nervi facialis
IXm, Nucleus motorius nervi glossopharyngei
Xm, Nucleus motorius nervi vagi
trigemini
n l
telenc
dienc
tect
corp cereb
auric
n V
n lat ant
nVl l l
1
6
r h o m b
n
X
n lat
post
nX
n spin
2
Fig. 1 Dorsal view of the brain of the axolotl Ambystornu mexiccinum
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B R A I N STEM
OF A M B Y S T O M A 289
pletely; however, a short groove, labeled
“a” in figures 9 and
13
may well represent
its most rostral part. This would be in
accordance with the findings of Rothig
(‘27)
in Cryptobranchus as well as with
our own observations in Rana e sc u l e n ta
(Opdam et al., ’75). There is no evidence
that the sulcus limitans extends into the
mesencephalon.
A sulcus in termedius dorsal i s is present
in the intermediate part of the rhomben-
cephalon. Its caudal part is shallow (figs.
4,
5), but its rostral part, which is situated
at the level of entrance of the VIIth and
VIIIth cranial nerves, is quite distinct (figs.
6,
7). Rothig (’27) and Kreht (’30) have
reported the presence of this groove in
Cryptobranchus , S i ren
and
Salamandra.
According to both of these authors
i t
sep-
arates the visceral sensory area from the
somatic sensory area. Judging from the
figures of Herrick (’30) the sulcus inter-
medius dorsalis is also present i n Ne c turus .
The su l c us m e d ianus supe r ior marks
the dorsal line of fusion of the lateral
walls of the neural tube. It is deep and
distinct throughout the larger part of the
mesencephalon (figs. 10, 11).
A well-marked sulcus passes in the ros-
tral part of the brain stem from rostro-
ventral to dorsocaudal over the ventricular
surface. This sulcus, which marks the
boundary between the tegmentum mesen-
cephali and the tegmentum isthmi, was
designated by Herrick (’17, ’35) as the
s u l c u s i s t h m i (figs. 9, 10). We also have
adopted this term.
The sulcus la teral is mesenceph al i marks
the widest extent of the mesencephalic
ventricular cavity.
A s
Herrick
(‘48)
has
pointed out, the boundary between the
tectum and the tegmentum mesencephali
is situated far below this sulcus (figs. 11,
13).
Subdiv i s ion of g r a y m a t t e r
Figures 2-12 show that in the brain
stem of A m b y s t o m a the somata of the neu-
rons constitute a continuous zone of peri-
ventricular gray. Within this periventric-
ular layer a certain number of more or
less individualized cell masses can be de-
limited, but no complete parcellation is
possible. The delineation of these cell mass-
es has been carried out with the help of
several criteria. The small, granular cells,
which make up the bulk of the gray mat-
ter show in the Bodian material employed
hardly more than their nuclei. Hence, the
usual cytoarchitectonic criteria are not ap-
plicable to them. However, local differences
in density
or
arrangement of the nuclei
of these small elements allowed us to draw
some borderlines. The larger neurons are
generally more completely impregnated and
for the delineation of areas constituted by
these elements size and shape of the so-
mata and the number and direction of the
dendritic trunks could be taken into consid-
eration (figs. 12a,c,d). Finally, by tracing
the root fibers of the efferent cranial
nerves toward their site of origin in the
central gray, the location of some motor
nuclei could be determined.
1. Som at i c m otor nuc l e i
The somatic efferent cell masses
of
the
brain stem include the most rostral part
of the spinal motor column and the moto-
neuronal groups which supply the external
eye muscles, i .e. , the abducens, trochlear
and oculomotor nuclei. All of these nuclei
lie close to the median plane in the outer
zone of the periventricular gray.
The
s p i n a l m o t o r c o l u m n ,
which con-
tinues for some distance rostrally to the
obex, consists of large (39 pm) and me-
dium-sized (27 pm) cells, with very well
impregnated dendritic trunks. According
to Herrick (’30) the most rostral part of
this column can be marked off from the
remainder and constitutes a primordial
hypoglossal nucleus. We remained unable
to confirm this observation.
The nuc le us ne ru i abduc e n t i s . The roots
of the nervus abducens could be traced
toward the most ventromedial part of the
stratum griseum, where an ill-defined
group
of
medium-sized cells
(16
pm)
could be identified as the nucleus of origin
of that nerve. This nucleus is indicated by
Herrick (’14) in A m b y s t o m a t i g r i n u m as
occupying a somewhat more rostral posi-
tion. In N e c t u r u s Herrick
(‘30)
misinter-
preted a part of the nucleus raphes as the
abducens nucleus.
The nuc leus nerui t rochlear is is repre-
sented by a group of medium-sized cells
(17 pm), situated in the isthmus region,
lateral to the deepest point of the sulcus
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290 P A U L OPDAM
AND
RUDOLF
NIEUWENHUYS
medianus inferior (fig. 10). The elements
of this group are rather diffusely arranged,
but are distinguished by their larger size
from the cells in the surrounding gray.
The
nuc le us ne rv i oc u lom otor i i
lies rath-
er far removed from the nucleus of the
trochlear nerve, but otherwise corresponds
closely to this cell mass with regard to
position, size (20 pm) and arrangement
of its cells (figs.
11
12b).
Our findings concerning the position and
appearance of the nuclei of the third and
fourth cranial nerves are in accordance
with those of Herrick (‘17, ’48), Kreht
(‘30, ’40b) and Leghissa (’49) in a variety
of urodelan species.
2. Visceral motor n uc le i
The visceral motor nuclei, i.e., the ef-
ferent centers of X IX, VII and V consti-
tute an almost continuous column of me-
dium-sized cells (18-22 pm . In Bodian
preparations the elements of this column
which, in general are rather diffusely ar-
ranged, are recognizable by their ventro-
laterally directed dendrites.
The nuc le us m otor ius ne rv i vagi and
the nuc le us m otor ius n e rv i g lossophary ng ii
constitute together a single cell mass, the
elements of which measure on the aver-
age 21 pm. This cell mass is situated in
the lateral part of the basal plate and
extends from the level of emergence of
the abducens roots into the most caudal
part
of
the rhombencephalon (figs. 3-5,
13). Herrick (’30, ’48) and Leghissa (’49)
claimed that the most rostral part of the
cell mass under consideration contributes
fibers to the facial nerve and thus repre-
sents a nucleus motorius nervi facialis,
pars caudalis. We remained unable to con-
firm these observations.
The n u c l e u s m o t o r iu s n e m i fa c ia l is is a
rather diffuse cell mass, situated rostro-
medial to the. Mauthner neuron (fig. 7).
Its cells are somewhat smaller than those
of the other visceral motor nuclei; they
measure on the average 18 pm. Our find-
ings with regard to the position and extent
of this nucleus (cf. fig. 13) are in agree-
ment with those of most previous authors
(Barnard, ’36; Herrick, ’48; Leghissa, ’49).
It is, however, noteworthy that according
to Kreht (‘40a) this nucleus is situated
close to the median plane.
The cells of the n u c l e u s m o t o r i u s n e r v i
t r i ge m in i
are medium-sized (22 pm) and
constitute a large and clearly defined unit
(figs.
8,
13). Herrick (’30) and Leghissa
(’49) distinguished within this nucleus a
rostral and a caudal moiety, but we found
no grounds for such a subdivision.
3.
Form atio ret icularis
For convenience of description the re-
ticular formation will be divided into three
longitudinal zones: (1) a median zone, con-
sisting of cells located in or near the raphe,
(2) a medial zone, which includes, in ad-
dition to a considerable area in the rhomb-
encephalic basal plate, a center in the
most rostral part of the tegmentum mes-
encephali, and (3) a lateral zone.
The m e dian re t i c u lar zone . Through-
out almost the entire extent of the rhomb-
encephalic raphe area scattered, small cells
(14 pm) occur. Between the levels of en-
trance of the trigeminal and vagus nerves
these elements are somewhat more com-
pactly arranged and may be designated as
the n u c l e u s r a p h e s . Apart from the small
elements already mentioned this nucleus
contains dispersed medium-sized (19 pm)
cells (figs. 4-8, 13).
The rhombencephalic part of the m e -
dial re t icular zone begins at a short dis-
tance from the median plane and borders
laterally upon the nuclei of the visceral
motor column. It consists of medium-sized
and large cells, and is situated in the ex-
ternal part of the central gray (figs. 3, 4,
6-8 . The large elements are generally
provided with horizontally arranged main
dendrites from which side branches ex-
tend into the white matter (fig. 12c). In
the previous section i t has been mentioned
that all conspicuous neuronal perikarya
in the reticular formation were measured
and that those measuring 19-35 pm (“in-
termediate reticular cells”) and those
larger than
5
pm (“large reticular cells”)
were plotted in the topological map (fig.
13). This analysis has revealed that the
zone under consideration contains a dis-
tinct, caudal concentration of intermediate
cells and, more rostrally, a second concen-
tration, composed of intermediate and large
elements. The former has been designated
as the nuc leus re t icular i s in fer ior , the lat-
ter as the nuc le us ret ic u lar is m e d ius . The
nucleus reticularis inferior is roughly co-
extensive with the motor nucleus of x;
the nucleus reticularis medius is situated
at the level of entrance
of
VIII. Similar
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B R A I N
STEM OF
A M B Y S T O M A
291
concentrations of large reticular elements
have been described under the same names
in the lamprey (Nieuwenhuys, ’72), car-
tilaginous fishes (van Hoevell, ’1
1
Smeets,
’73),
Lat im e r ia (Kremers,
’76)
and in var-
ious reptiles (van Hoevell, ’11; ten Don-
kelaar and Nieuwenhuys,
’76).
No equiv-
alent of the nucleus reticularis superior,
a group of large elements which, in the
groups and species just mentioned, lies in
front of the motor nucleus of
V
has been
observed in the axolotl. The rhombence-
phalic medial reticular zone, as described
here, corresponds to the nucleus motorius
tegmenti of Edinger (‘08). The latter term
has been employed by Herrick (‘30) in his
extensive description of the rhombenceph-
alon of
N e c t u r u s .
It is, however, note-
worthy that Herrick, contrary to Edinger,
included in this nucleus not only the larger
and more conspicuous reticular elements,
but also a considerable part of the small-
celled periventricular gray of the basal
plate.
The mesencephalic part of the medial
reticular zone is represented by the nu-
c l e us of t h e f asc i c u lus l ong i tud ina li s m e -
dialis, a group of rather loosely arranged,
medium-sized cells (26 pm), situated in
the superficial zone of the tegmental gray.
As shown in figure 12d, its neurons are
provided with one or more laterally ex-
tending dendritic trunks.
In the mam-
malian rhombencephalon the area situated
between the medial reticular formation
and the nucleus of the tractus descendens
nervi trigemini is occupied by a zone of
small cells, which has been termed the
nucleus reticularis parvicellularis or the
lateral part of the reticular formation. In
reptiles diffusely arranged cells occupy a
corresponding position (Cruce and Nieu-
wenhuys, ’74; ten Donkelaar and Nieu-
wenhuys,
’76). A
probable amphibian
homologue of the nucleus reticularis par-
vicellularis has been observed by Herrick
(‘30)
in Ne c turus . For this species Herrick
described under the name “reticular for-
mation” an ill-defined area, situated be-
tween the sensory field and the motor field
of the rhombencephalon. According to that
author this area represents “a primitive
sort of correlation tissue,” concerned chief-
ly with the organization of bulbar reflexes.
Later, Herrick (‘48, A m b y s t o m a ) consid-
ered this reticular formation as a part of
The lateral re t icular zone.
an “intermediate zone,” which he believed
to extend throughout the brain. In the
axolotl the periventricular gray contains
doubtless an equivalent of the “reticular
formation” as observed by Herrick. How-
ever, delimitation of such a lateral retic-
ular zone on a cytoarchitectonic basis ap-
peared to be impossible.
4. Visceral sensory n uc le i
Herrick (’44) has pointed out that in
A m b y s t o m a all visceral afferent compo-
nents of the cranial nerves, the general
as well as the special or gustatory ones,
converge into the fasciculus solitarius. The
latter constitutes a conspicuous bundle in
the caudal part of the rhombencephalon
(figs.
2-5).
The small cells
(13 Fm)
which
surround this bundle may be designated
as the nu c le us fusc icul i so l itar ii . This “nu-
cleus” cannot be delimited from the adja-
cent gray, yet in order to indicate its
approximate position the contour of the
fasciculus solitarius has been included
in the chart (fig.
13).
The isthmus region contains a group
of scattered, small cells (13 pm), which
is situated lateral to the periventricular
gray and just ventral to the level of the
sulcus isthmi (fig.
9).
The cells in its most
lateral parts are in places more densely
packed than the more medial ones. This
cell group corresponds to the nuc leus u is -
ceral i s secundar ius , described by Herrick
(’17, ’48) and Barnard
(‘36).
According
to the authors just mentioned this nucleus
receives the fibers of a secondary visceral
tract which arises from the nucleus fas-
ciculi solitarii.
5. General somat ic sensory nuc le i
In
urodeles three nuclei related to the
sensory component of the trigeminal nerve
are known, uiz . the nucleus princeps
the nucleus tractus descendens and the
nucleus mesencephalicus nervi trigemini.
A nu c le u s pr ince ps ne rv i t r i ge m in i has
been observed by Herrick
(’30)
and Wood-
burne (‘36). According to the former this
nucleus is represented by an area of neu-
ropil containing outlying cell bodies, which
is associated with the ascending sensory
V root. The latter author indicated that
this nucleus cannot be sharply delineated,
but that its constituent cells are slightly
larger than those
in
the surrounding gray.
A primordial nuc le us t rac tus de sc e nde ns
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292
P A U L O P D A M A N D R U D OL F N I E U W E N H U Y S
nerui t r igemini
has been described by Her-
rick (’30), as follows: “Ventrally of the
VIII nucleus and confluent with it there
is an obscure differentiation of the gray
substance which represents the incipience
of the sensory
V
nucleus. It contains both
small and large cells, the former more
numerous at the level of the calamus sc ri p
torius and below it. There is also a group
of larger cells in the vagus region.” Ac-
cording to Woodburne (‘36), who studied
N e c t u r u s , A m b y s t o m a as well as Siren
material, the nucleus in question is ex-
tremely sparse, consisting of a few small
cells interspersed between the fibers of
the descending root. In our material of
A m b y s t o m a m e x i c a n u m neither a nucleus
princeps, nor a nucleus tractus descendens
nervi trigemini could be distinguished. The
nuc le us m e se nc e pha l i c us ne ru i t r i ge m in i
on the other hand is very conspicuous in
the axolotl. Its large cells (27 pm) are
scattered throughout the length of the tec-
tum (figs. 9-11, 12a, 13). Some of its ele-
ments are situated in the velum medullare
anterius. Our observations with respect to
this nucleus agree with those of Kings-
bury (1895), Herrick (’17,
’30)
and Kreht
6. Special somat ic sensory and
cerebel lar nuclei
According to Herrick (’14, ’30, ’48) and
Larsell (’67) a considerable part of the
white matter of the rhombencephalic alar
plate is occupied by primary afferent fi-
bers of the VIIIth and of the lateral line
nerves. On entering the brain these fibers
bifurcate into ascending and descending
branches. The ascending branches reach
the cerebellar region, the descending ones
extend to the level of entrance of the
vagal roots (fig. 1). The lateral line nerve
fibers constitute a number of bundles in
the dorsal part of the alar plate. The
cells in the adjacent gray extend their
dendrites into these bundles, thus consti-
tuting the area lineae lateralis (area acu-
stica of Herrick, ’30, ’48). Throughout the
larger part of its extent the ventral bound-
ary of this area is indicated by a ven-
tricular groove, the sulcus intermedius
dorsalis (figs. 4-7, 13). Only the stretch
of the area lineae lateralis, situated be-
tween the levels of entrance of the anterior
and posterior lateral line nerves, shows a
(’37).
tendency toward differentiation into s e p
arate cell masses (fig. 12e). In that region
the most dorsal part of the periventricular
gray shows a local condensation which
may be termed the nuc leus dorsal i s areae
octavolateral is .
Its cells are small (13 pm)
and do not differ
in
size from those in the
adjacent gray. More ventrally, a group of
cells of the same size can
be
delimited
from the inner zone of the periventricular
gray. This group is designated here as the
nuc le us i n t e r m e d ius are ae oc tav o la t era li s.
Its cells tend to surround a small area
devoid of cells. Both of these nuclei pass
rostrally as well as caudally gradually over
into the undifferentiated gray of the area
lineae lateralis. The names nucleus dor-
salis and nucleus intermedius areae oc-
tavolateralis have been used because these
nuclei correspond in position and afferent
connections to the cell masses of the same
name, found in various groups of fishes
(Smeets and Nieuwenhuys, ’76; Thors and
Nieuwenhuys, ’76, in preparation; Kre-
mers and Nieuwenhuys, ’76, in prepara-
tion).
The fibers of the eighth nerve enter
the brain ventral to the anterior lateral
line nerve. Their ascending and descend-
ing branches form bundles which are sit-
uated directly dorsal to the fibers of the
trigeminal nerve. Herrick (‘30) and Lar-
sell (‘67) observed that cells of different
sizes enter into synaptic relation with the
octavus fibers. The largest elements of
the octavus area constitute an elongated
column of medium-sized cells (26 pm),
situated in the outer zone of the central
gray (figs.
5-7,
12e). The caudal part of
this cell column is separated from the
gray of the area lineae lateralis by the
fasciculus solitarius (fig. 13). Herrick
(’30)
called the cell group in question the VIII
nucleus. Since we consider it homologous
to the nuc leus ves t ibular i s magnoce l lu lar i s
of various groups of fish, we have desig-
nated it by that name.
The soma of the giant
cell
of
M a u t h n e r
(93 pm) is situated immediately medial
to the magnocellular vestibular nucleus.
Like the elements of the latter the Mauth-
ner cell extends the branches of its lateral
dendrite toward the entering octavus
fi
bers. It should be mentioned parentheti-
cally that the
A m b y s t o m a m e x i c a n u m
specimen employed for the preparation of
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B R A I N STEM OF A M B Y S T O M A
293
the topological chart (fig. 13) happened
to have only a Mauthner cell on the right
hand side. All other specimens studied
showed two, bilaterally symmetrical giant
elements.
The rostra1 part of the area lineae lat-
eralis and of the adjacent area octavi con-
sists entirely of undifferentiated gray. An-
teriorly these areae pass over into the
cerebellum and into a small intraventric-
ular protrusion known as the eminentia
subcerebellaris tegmenti. This protrusion
is ventrally bounded by the sulcus “a”
(fig. 13). In the superficial part of its
periventricular gray a group of small cells
(12 pm) can
be
delimited. With Herrick
(’48)
we consider this cell group as a
primordi a1
nucleus cerebe li.
7. Nuclei of the isth mus region
The nucleus interpeduncularis is con-
stituted by diffusely arranged, small cells
(13 pm), situated in and near the raphe.
As Herrick (’34) has pointed out, this cell
mass comprises a small anterior and a
much larger posterior part. The anterior
part is situated directly caudal to the level
of the oculomotor nuclei. The posterior
part begins in front of the trochlear nu-
clei and extends caudally to the level of
the trigeminal roots.
A group of scat-
tered, small cells (14 pm), situated lateral
to the central gray and just dorsal to the
sulcus isthmi most probably represents the
homologue of the nucleus isthmi of anu-
rans and of various groups of fish (Smeets
and Nieuwenhuys, ’76; Thors and Nieu-
wenhuys, ’76, in preparation).
The nucleus isthmi.
DISCUSSION
In the preceding section the ventricular
sulcal pattern and the cell masses in the
brain stem of the axolotl
Ambystoma mexi
canum have been described. Leaving aside
some very short grooves it may be stated
that the rhombencephalon contains five
longitudinal sulci, namely the sulcus limi-
tans, the sulcus intermedius ventralis and
dorsalis and the sulcus medianus ventralis
and dorsalis. The two sulci last mentioned
can also
be
distinguished in the mesen-
cephalon and this region contains another
longitudinal groove, the sulcus lateralis
mesencephali. In the transitional area
of
the rhombencephalon and the mesenceph-
alon an obliquely oriented sulcus isthmi
clearly diverges from the overall longitu-
dinal pattern of the sulci. Nineteen nu-
clear masses have been delineated. Sixteen
of these are embedded in the central gray;
only three,
viz.
the nucleus interpeduncu-
laris, the nucleus visceralis secundarius
and the nucleus isthmi, consist of neurons
that have migrated outward into the stra-
tum album. Eleven out of the
19
cell
masses represent cranial or spinal nerve
nuclei; seven of these are primary effer-
ent and four are primary afferent centers.
Four nuclei can be regarded as compo-
nents of the reticular formation. The re-
maining four nuclei may be interpreted
as “relay” nuclei. This category includes
the three migrated nuclei mentioned above
plus the nucleus cerebelli.
As has been pointed out in the intro-
duction, the present paper forms part of
a program of research within the frame
of which the morphological pattern of the
brain stem will be studied in a number
of representative vertebrates. For a de-
tailed discussion of this program and its
aims the reader is referred to Nieuwen-
huys (’74). Suffice i t to mention here that
for each species studied the validity of
the following four statements will be tested.
1 . The lateral wall of the brain stem
consists of two longitudinal plates, the
dorsally situated, primarily sensory alar
plate and the ventral, primarily motor ba-
sal plate. The basal and alar plates are
separated from each other by a ventricular
groove, the sulcus limitans (His,
1888,
1893a,b).
2.
The grisea in the basal and alar
plates are arranged in two longitudinal
columns or areas. The basal plate contains
a medial area ventralis and a lateral area
intermedioventralis; the alar plate con-
tains a ventral area intermediodorsalis and
an area dorsalis. The boundaries between
the two zones contained within both the
basal and the alar plate are generally
marked
by
two ventricular grooves, the
sulcus intermedius ventralis and inter-
medius dorsalis respectively (Kuhlenbeck,
’26, ’27).
3. Within the rhombencephalon the pri-
mary efferent and afferent centers are
arranged in four longitudinal columns.
These are, from ventromedial to dorsolat-
eral, the somatic motor, visceral motor,
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294 PAUL
OPDAM
AND
RUDOLF
NIEUWENHUYS
visceral sensory and somatic sensory zone
(Herrick, 1899, ’13; Johnston, ’01,
’02).
4. Certain centers of higher order (des-
ignated as motor coordination nd sen-
sory correlation centers) also fit into the
pattern of the “functional” zones men-
tioned sub 3
e . g . ,
Herrick, ’13; Bartel-
mez, ’15; Tuge, ’32).
A s regards the applicability of these
statements to the brain stem of A m b y s -
t o m a m e x i c a n u m the topological analysis
represented in figure 13 warrants the fol-
lowing conclusions.
Throughout
the caudal two-thirds of the rhombenceph-
alon a sulcus limitans is present. In the
rostral one-third this sulcus is lacking, but
the subcerebellar sulcus “a” may well
represent a rostral continuation of the
sulcus limitans. If this interpretation is
correct, most of the rhombencephalon is
divisible into a basal plate and an alar
plate. However in the mesencephalon a
ventricular landmark for making this sub-
division is entirely lacking. The designa-
tion of the basal plate as “motor” and
the alar plate as “sensory” is correct in
so
far that all primary efferent centers
are situated within the former and all pri-
mary afferent centers within the latter.
Within the
basal plate a medial area ventralis and a
lateral area intermedioventralis can be
easily discerned. The area ventralis com-
prises the rostral part of the spinal motor
column, the abducens nucleus, the troch-
lear nucleus, the rhombencephalic part of
the medial reticular formation and one
half of the nucleus raphes and of the
nucleus interpeduncularis. The area in-
termedioventralis is constituted by the
motor nuclei of V VII, IX and
X. A
sulcus
intermedius ventralis, delimiting the area
ventralis from the area intermedioventralis
is present only in the most caudal part of
the rhombencephalon.
The functional designation of the area
ventralis as the somatic motor column is
appropriate in the sense that it contains
three somatic motor centers: the rostral
end of the spinal motor column and the
nuclei of VI and IV. However, the remain-
ing nuclei in this area cannot be regarded
as purely somatic motor. The nucleus in-
terpeduncularis has been characterized by
Herrick (‘48) as a “motor pool in Sher-
rington’s sense”; yet the efferents of this
Basal pla te lar p la te .
Subdiv i s ion of basal plate .
nucleus discharge according to the author
mentioned not only into the somatic motor,
but
also into the visceral motor nuclei of
the rhombencephalon. The medial retic-
ular zone has been considered by various
authors, among them Herrick ‘30), to
represent a somatic motor coordination cen-
ter, the axons of which descend in or
near the fasciculus longitudinalis medi-
alis to the spinal cord. However, Herrick
(’39,
’48)
later demonstrated that axons of
large reticular elements bifurcate into long
ascending and descending branches. As in
mammals, the ascending branches may
well be a link in a nonspecific projection
to the thalamus and to other prosence-
phalic structures. If
so
the designation
of the medial reticular zone as a whole
as “motor” in inappropriate.
All of the nuclei present in the area
intermedioventralis belong to the visceral
motor category. Hence, so far as its delim-
itable cell masses are concerned, this area
may be aptly designated as the visceral
motor column.
Subdiv i s ion
of
alar plate .
A
distinct
sulcus intermedius dorsalis divides the
intermediate part of the alar plate into an
area intermediodorsalis and an area dor-
salis. The area intermediodorsalis contains
two cell masses, the nucleus vestibularis
magnocellularis and the nucleus fasciculi
solitarii. The latter extends into the caudal
part of the rhombencephalon, where i t
occupies almost the entire height of the
alar plate. We consider it likely that the
region situated directly dorsal to the sulcus
“a” represents a rostral continuation of
the area intermediodorsalis. Figure 13
shows that in this region two cell masses
are present, the nucleus cerebelli and the
nucleus visceralis secundarius. The area
dorsalis contains mainly undifferentiated
gray and only in a short segment of i t
can two cell masses be delimited. These
have been termed here the nucleus dor-
salis and the nucleus intermedius areae
oc tavolater alis.
From the data presented above it ap-
pears that the area intermediodorsalis is
not equivalent to the visceral sensory zone.
The latter is represented by the nucleus
fasciculi solitarii and the nucleus viscera-
lis secundarius. However, the nucleus ves-
tibularis magnocellularis belongs to the
special somatic sensory category and the
nucleus cerebelli is a relay center which
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BRAIN STEM OF
A M B Y S T O M A 295
cannot be characterized as either “sen-
sory” or “motor.” Thus the constituents
of the intermediodorsal area do not con-
stitute a functional entity. It is noteworthy
that the caudal part of the nucleus ves-
tibularis magnocellularis i s separated from
the remaining special somatic sensory cen-
ters by the visceral sensory nucleus fas-
ciculi solitarii. Herrick (’14), who has al-
ready drawn attention to these remarkable
spatial relationships, supposed that a part
of the somatic sensory column has shifted
ventrally along the lateral surface of the
rhombencephalon.
According to the doctrine of the func-
tional columns (Herrick, 1899, ’13; John-
ston, ’01, ’02), he dorsal part of the alar
plate is constituted by a somatic sensory
zone, which can be subdivided into a ven-
tral general somatic sensory column and
a dorsal special somatic sensory column.
The latter is thought to contain the cen-
ters of termination of the eighth and the
lateral line nerves. In the rhombenceph-
alon of the axolotl no general somatic sen-
sory nuclei could be delimited. It is, how-
ever, important to note that, according
to the projection method employed in the
present-paper, the large tractus descen-
dens nervi trigemini lies partly in the alar
plate and partly in the basal plate. There-
fore it may be expected that the gray re-
lated to this bundle,
is
situated in the
vicinity of the sulcus limitans. The undif-
ferentiated gray and the two cell masses
situated in the area dorsalis receive their
input from the lateral line nerves. On that
account this area may be designated as a
special somatic sensory column.
Th e cerebellum
a n d
the
nucleus
isthmi.
If our interpretation of the sulcus “a” as
the most rostral part of the sulcus limitans
is correct, the cerebellum is a derivative
of the entire alar plate (fig. 13). Larsell
(’67) believed that the cerebellum is the
rostral continuation of the general and
the special somatic sensory columns. Since
we failed to delimit these two functional
columns in the rostral part of the rhomb-
encephalon, we are unable to take a stand
on this issue. As regards the nucleus
isthmi, lack of adequate landmarks pre-
cludes insertion of this cell mass into the
longitudinal zonal pattern.
Th e mesencephalon. The sulcus limitans
does not extend into the mesencephalon
and there is no evidence that the sulcus
lateralis mesencephali constitutes the ros-
tral continuation of this landmark. How-
ever, despite the absence of a distinct bor-
derline between the basal and alar plate it
may be stated that two functional zones,
the somatic motor and the somatic sensory,
are represented in the mesencephalon. In
the medial part of the tegmentum mesen-
cephali the nucleus nervi oculomotorii and
the nucleus of the fasciculus longitudi-
nalis medialis constitute the rostral ex-
treme of the somatic motor column. (In
this interpretation i t is taken for granted
that the nucleus of the f.1.m. indeed dis-
charges its axons into the bundle after
which it is named and, thus, may be
interpreted as a somatic motor coordina-
tion center.) The tectum mesencephali may
be designated as both a primary somatic
sensory center and a somatic sensory cor-
relation area. The former because it con-
tains the nucleus mesencephalicus nervi
trigemini; the latter because it has been
shown to receive projections from the eyes
(Jackway and Ris, ’72) and from the spinal
cord (Nieuwenhuys and Cornelisz, ’71).
ACKNOWLEDGMENTS
The authors wish to thank Dr.
L.
H.
Bannister for critically reading the manu-
script. We are also grateful to Mrs. G . van
Son-Verstraeten for her secretarial assist-
ance, to Mrs.
C.
de Vocht-Poort and Miss
P. Verijdt for their histological work,
to
Mr. J. Konings for the drawings and to
Mr. A. Reijnen for the photomicrographs.
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Opdam, P. , M Kemali and R. Nieuwenhuys
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PLATES
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PLATE
EXPLANATION
OF FIGURES
2-7
Transverse sections
of
the rhombencephalon
of
the axolotl Ambystomo
mexictinzim.
The levels
of
these sections hav e been indicated i n fig
ures
1
and
13.
Bodian stain,
X
40.
298
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B R A I N STEM OF
A M B Y S T O M A
P a u l Opdam a n d Rudolf Nieuwenhuys
P L A T E 1
299
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PLATE 2
EXPLANATION OF
FIGURES
8-1 1
Transverse sections
of
the rostra1 rhombencephalon and the mesen-
cephalon of the axolotl
Am bys torm mc xictinimz.
The levels of these
sections have been indicated in figures
1
and
13.
Bodian stain.
X
40.
300
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BRAIN STEM
OF
AMBYSTOMA
P a u l Opdarn and R u d o l f N ieu wen h u y s
PLATE 2
30
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P1.ATE 3
EXPLANATION
OF
FIGURES
12a-e
Deta ils of som e nuclei in the brain stem of the axolotl Ambystorno
mc xic-rr?r?im.
Bodi;iii stain. a . Two cells of the nuc leus mesencephal
iccis iiervi trigcniini. X
220.
b. Nucleus nervi oculomotorii shown
‘tt rhc.
ic.vr~lof
emerycnrt’ of
its
roots.
X
1 1 0 .
c. Large element
of
t h r riuclcus r(,ticularis
i r i r d ~ u s .
X
350. d.
N U C ~ L I Sf the fasciculus
longi tud inal i s ind ial i s . X
220.
e. Transverse section of the alar
plat<,
,just beind thc level of entra nce of the eighth nerve. x 110.
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BRAIN STEM OF AMBYSTOMA
Pau l Opdam
and Rudolf Nieuwenhuys
PLATE 3
303
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PLATE 4
E X PL A N A T I O N
O F
FIGURE
13
Topological reconstruction of the brain stem of the axolotl A,tnhystomo
mc>xicctrzirm. The heavy line which constitutes the axis of the figure
represents t he sulc us median us inferior. The curves which constitute
the lateral limits of the figure represent the taen ia rhombencephali
(con tinuo us parts) an d the sulcus median us superior (dashed parts).
The rema ining sulci are indicated by heavy curves. The thin , cont in-
uous curves
indicate the boundaries
of
periventricular cell masses;
the outlines
of
migrated nuclei are indicated by th in, interrup ted
curves. T he delimitable parts of the reticular formation ar e indicated
by curves of alt ern ate dots and dash es
.
). The filled-in circles
give an impression of the distributio n a nd density of the large an d
interniediatc reticular cells 1 out of 3 cells of both
of
these ca te~
gories has been indicated). The open circles represent the elements of
the nucleus mesencephalicus nervi trigemini.
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BRAIN STEM
O F
A M B Y S T O M A
Paul Opdam and Rudolf Nieuwenhuys
\
P L A T E 4
siv