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



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-



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-



288


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



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



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



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



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



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,



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



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



PLATES



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



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



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



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



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.



BRAIN STEM OF AMBYSTOMA

Pau l Opdam

and Rudolf Nieuwenhuys

PLATE 3

303



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.



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

Opdam Et Al-1976-Journal of Comparative Neurology

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Transcript of Opdam Et Al-1976-Journal of Comparative Neurology