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THE SUPERIOR AND INFERIOR COLLICULI O F THE
MOLE (SCALOPUS AQUATICUS MACHXINUS)
THOMAS N. JOHNSON' Laboratory o f Comparative Neurology, Departmmt of Amtomy, Un&versity of hfiehigan, Ann Arbor
INTRODUCTION This investigation is a study of the afferent and efferent
connections of the tectum of the midbrain in the mole (Scalo-
pus aquaticus machrinus). An attempt is made to correlate
these findings with the known habits of the animal.
A subterranean animal of the middle western portion of the
United States, Scalopus aquaticus machrinus is the largest
of the genus Scalopus and its habits have been more thor-
oughly studied than those of others of this genus according
to Jackson ('15) and Hamilton ('43). This animal prefers
a well-drained, loose soil. It usually frequents open fields
and pastures but also is found in thin woods and meadows.
Following a rain, new superficial burrows just below the
surface of the ground are pushed in all directions to facili-
tate the capture of worms and other soil life. Ten inches
or more below the surface the regular permanent highway
is constructed; the mole retreats here during long periods
of dry weather or when frost is in the ground. The principal
food is earthworms although, under some circumstances,
larvae and adult insects are the more usual fare. It has been
demonstrated conclusively that, under normal conditions,
moles will eat vegetable matter. It seems not improbable
that they may take considerable quantities of it at times.
A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the University of Michigan. 1952. 765
766 THOMAS N. JOHNSON
The single annual litter suggests that moles have few enemies. Their fossorial habits prevent hawks and owls from taking any considerable numbers in spite of the fact that the moles are active at all hours. Nevertheless they do
fall prey to predatory birds and mammals.
Reed ('51) described the manner of locomotion. The great-
est power is exerted by the mole when the forefeet are thrust
out directly laterally; it employs them in this manner when
digging the shallow burrows in which the soil is thrust up in a ridge. The mole rotates in its burrow and, thrusiing from below with one forefoot, raises the roof of the burrow
with the other. Then the animal rotates its whole body M O O ,
or nearly so, and repeats the process. I n excavation of deeper burrows, in which the roof cannot be elevated, only one fore- foot is used at a time, while the other is braced against the side of the burrow. The earth is loosened by lateral strokes of first one forelimb and then the other, the earth being
thrown back beside and beneath the body. After a period
of such activity the mole then turns around in the newly formed burrow, the diameter of which is scarcely more than
that of its own body, and proceeds to shove the dirt out,
using one outthrust forefoot as a pusher, with the neck and
thorax bent to one side and locomotion achieved by use of
the other three limbs; this same posture is maintained when
pushing dirt out onto the surface. Under such conditions the hind limbs are performing the major part of the locomotor
effort. Out of its burrow the mole is a clumsy animal, pro-
gressing awkwardly by running with its hind legs while trying to support the heavy front part of the body on its outstretched front legs, which are in contact with the ground only on the edge of the thumb. The microscopic study shows a poorly developed optic
system, a well developed acoustic system and a smaller su-
perior than inferior colliculus. The other afferent and efferent fiber connections of the midbrain generally conform to those of other insectivores, rodents and marsupials.
768 THOMAS N. JOHNSON
mals in a series of papers. The work of Ariens Kappers,
Huber and Crosby ('36) includes a thorough account of the
structure and fiber connections of the midbrain for a series
of mammals.
The more recent work of Huber et al. ('43) contributed
much to the knowledge of the nuclear groups of the tegmental
portions of the mammalian midbrain from the marsupial to
man. Woodburne, Crosby and McCotter ('46) described the
connections of the basal ganglia with the midbrain tegmentum
in the macaque. Later experimental work by Crosby and
Henderson ( '48) established certain cortico-tectal connections
of the superior colliculi in the macaque and the relation of
these centers to automatic eye movements.
Tsai ('25a) traced the optic tracts in the opossum. Brouwer
('27) described the projection of the retina on the superior
colliculus of the rabbit and Lashley ('34) demonstrated the
distribution of optic tract fibers in the superior colliculus
of the rat. Barris, Ingram and Ranson ('35) described the
optic connections of the diencephalon and midbrain of the
cat. Gillilan ( '41) reported the connections of the basal optic
root in the shrew and found that this pathway was not so
reduced as the optic tract. Many observers have described
the optic system in higher mammals.
The gross structure of the brain of various European in-
sectivora has been described by Le Gros Clark ( '33). Other
references related to the various fiber connections of the
midbrain will be incorporated in the description of the ma-
terial and in the discussion.
NUCLEAR PATTERN O F THE TECTUM
The Nuclear patterm of the ilzferior colliculus
The nucleus of the inferior colliculus is very large in this
animal (fig. 9). I n it can be recognized a central nucleus
with large multipolar cells the axons of which pass through
the brachium of the inferior colliculus to enter the medial
geniculate nucleus. This central nucleus is surrounded by a
MIDBRAIN OF THE MOLE 769
fibrous capsule which is formed by the fibers of the lateral
lemniscus and the peduncle of the inferior colliculus together
with cells continuous with the outer layers of the superior
colliculus as they turn into the nucleus (fig. 9). The chief
nucleus is continuous with the periventricular gray of the
area in front of it.
The Euyerircg of the superior colliculus
Although many of the layers of the optic tectum are re-
duced, 8 layers (figs. 4 and 5) can be distinguished in the optic
tectum of the mole.
1. Stratum xomale. This layer is very thin and is composed
of a small number of external cortico-tectal fibers. Ganser
(1882) did not demonstrate this layer in the mole. It corre-
sponds to w1 of Frankl-Hochwart ('02) for Spalax typhlus
(a European mammal corresponding to the American gopher)
and to the stratum zonale of Winkler and Potter ('11and '14)
for the rabbit and cat, Tsai ('25b) for the opossum, and Huber
and Crosby ('43) for mammals in general.
2. Stratwm griseum superficiale. This area consists of
small and medium-sized cells and some of the endings of the
external cortico-tectal fibers. It corresponds to the oberflach-
liches Grau of Ganser (1882) for the mole, gl of Frankl-
Hochwart ('02) for Spalax typhlus and the stratum griseum
superficiale of Winkler and Potter ('11 and ,14) for the
rabbit and cat, Tsai ('25b) for the opossum and Huber and
Crosby ('43) for mammals in general.
3. Stratum opticurn. This area is extremely minute with
small bundles of optic tract fibers which split as they enter
the tectum and terminate medially and laterally. This layer is
comparable to the oberflachliches Mark of Ganser (1882) for
the mole, w, of Frankl-Hochwart ('02) for Spalax typhlus,
to the stratum medullare superficiale of Winkler and Potter
('11 and '14) for the rabbit and cat, and to the stratum op-
ticum of Tsai ( '25b) for the opossum and Huber and Crosby
( '43) for various mammals.
MIDBRAIN OF THE MOLE 771
sented in the tiefes Mark of Ganser (1882) for the mole, in
w, of Frankl-Hochwart ('02) for Spalax typhlus, in the
stratum medullare profundum of Winkler and Potter ('
and '14) for the rabbit and the cat, and in the stratum album
profundum of Tsai ('25b) for the opossum and Huber and
Crosby ('43) for mammals.
8. Stratum griseum periveattriculare pars dorsalis. This
layer contains medium- and small-sized cells with the finely
medullated and unmedullated acustico-optic fiber fascicles
interspersed among the cells. Most students of mammalian
brains have not considered the periventricular layers as a
part of the optic tectum. Crosby and Woodburne ('43) con-
sidered the pars dorsalis of the periventricular gray in the
shrew as part of the midbrain tegmentum. Tsai ('25b) re-
ferred to the periventricular gray in the midbrain of the
opossum as the substantia grisea centralis.
THE FIBER CONNECTIONS OF THE TECTUM
Agerent pathways to the tectum
Optic tract
Le Gros Clark ('33) found that a characteristic feature
of a number of insectivores is the very small optic nerve and
tract which are associated with a small lateral geniculate
body in which the ventral nucleus is larger and the dorsal
nucleus is smaller and poorly developed.
The optic chiasma (fig. 2) is microscopic in size as it lies
on the ventral surface of the diencephalon. It is not possible
to determine whether the optic tract crosses completely in
the chiasma in this material. The fibers sweep in a caudo-
lateral direction from the chiasma and then dorsolaterad
around the ventrolateral border of the diencephalon. As the
tract approaches the cerebral peduncle, fibers are given off
to the nucleus of the basal optic root. Gillilan ('41) studied
the optic tracts and basal optic root in the shrew and con-
cluded that reduction in size of the accessory optic tracts,
especially of the tractus opticus basalis or the basal optic
772 THOMAS N. JOHNSON
root, is not proportional to the reduction in size of the optic
tract. The present material would tend to document this
statement for the mole. At the dorsolateral region of the
diencephalon part of the fibers enter the lateral geniculate
ABBREVIATIONS AQ., aqueduct. BRACH. CONJ.. brachium con.juncti- vum. colliculus.
BRACH. I.C., brachium of the inferior BRACH. PONT., brachium pontis. CEREBR. PED., cerebral peduncle. COMM. INF. COL., commissure of the DEC. BRACH. CONJ., decussation of DEC. TRAP. FIB., decussation of trape- D. COCH. NUC., dorsal cochlear nucleus. D. NUC. LAT. LEMN., dorsal nucleus
D. NUC. RAPHE, dorsal nucleus of
D. TEG. DEC., dorsal tegmeiital decus-
EXT. CORT. TECT., external cortico.
HAB. PED. TR., habenulo-peduncular HYPOTHAL., hypothalamus. INF. COL., inferior colliculus. INF. THAL. RAD., inferior thalamic INT. CORT. TECT., internal cortico-
inferior colliculus. the brachium con junctivum. zoid fibers.
of the lateral lemniscus. raph6. sation. tectal tract. tract.
radiations. tectal tract. cleus.
INTERPED. NUC., interpeduncular nu- LAT. GEN. NUC., lateral geniculate nucleus. LAT. LEMN., lateral lemniscus. LAT. TECT.-SP., lateral tecto-spinal tract. nucleus.
MED. GEN. NUC., medial geniculate MED. LEMN.. medial lemniscus. MED. TECT.:SP., medial tecto-spinal M.L.F., medial longitudinal fasciculus. N1G.-TECT., nigro tectal tract. NUC., nucleus. NUC. DESC. RT. TRIG., nucleus of the descending root of the trigeminal. NUC. FAC., nucleus of facial nerve. NUC. TNF. COL., nucleus of the inferior colliculus. NUC. OCUL. N., nucleus of oculomotor nerve.
tract.
NUC. TROCH. N., nucleus of troehlear OP. CH., optic chiasm. OP. TR., optic tract. PERIV. GR., periveiitricular gray. PONS, pons. PONT. GR., pontine gray. PRETECT. AREA, preteetal area. PYR., pyramid. REST. BOD., restiform body. R. NUC., red nucleus. RT. FAC., root of the facial nerve. RT. TRIG. N., root of the trigeminal S. NIGRA, substantia nigra. SP.-TECT., spino-tectal tract. STR. ALB. PROF., stratum album pro- STR. ALB. INTERMED., stratum al-
nerve.
nerve.
fundum. bum intermediale. STR. GRIS. INTERMED.. stratum eri- seum intermediale. periventriculare.
STR. GRIS. PERIV., stratum griseum STR. GRIS. PROF., stratum griseuni prof undum. seum sunerficiale.
STR. GRIS. SUPERFIC., stratum gri- STR. OP+., stratum opticum. STR. ZON., stratum zonale. SUP. COL., superior colliculus. SUP. OL., superior olive. SUP. THAL. RAD., superior thalamic TECT.-NIGR., tecto-nigral tract. TECT.-PONT., tecto-pontine tract. TECT.-RUBR., tecto-rubral tract. TECT.-TEG., tecto-tegmental fibers. TRAP. FIB., trapezoid fibers. VENT. CAUD. NUC. LAT. LEMN., v&ntral caudal nucleus of lateral lem- V. COCH. NUC., ventral cochlear nu- cleus. VENT., ventricle. V. SEC. ASC. TR. TRIG., ventral sec- ondary ascending tract of trigeminal. V. TEG. DEC., ventral tegmental decus- sa tion. X. INC., zona ineerta.
radiations.
111scus.
774 THOMAS N. J O H N S O X
connections with the ventral nucleus of the lateral geniculate body in the cat, although it is true that many of these fibers pass through this nucleus as they approach the dorsal nucleus.
The optic tract in the mole, very small in size after it has
contributed fibers to the nucleus of the basal optic root and to the lateral geniculate nucleus, continues dorsocaudad (figs.
INF. THAL. RAD.
VENT. HYPOTHAL. Fig. 2 Photomicrograph of a transverse section passing through the rostra portion of the dieneeplialoii of the mole at the level of the optic chiasm. Silver preparation. X 30.
3 and 4) into the midbrain where the remaining fibers ter-
minate in the superior colliculus. As the optic fibers approach the superior colliculus, they divide so that some of them enter the tectum laterally and the others enter it medially, to repeat the pattern of mammalian optic fiber terminations in the tectum. The number of fibers contributed to the su- perior colliculus is very slight, nevertheless the superior
colliculus in the mole is well developed (figs. 1 and 4). Lash-
ley ('34) described a similar distribution of optic tract fibers
MIDBRAIN O F T H E MOLE 775
in the superior colliculus of the rat. In the r a t the temporal
quadrants of the retina are projected t o the anterolateral,
the nasal quadrants to the posteromedial portions of the superior colliculus ; the upper quadrants are projected laterad to the lower quadrants. Brouwer and Zeeman ('26) were unable to establish the pattern of projection of the retina on the superior colliculus of the cat because, according to their own statement, their material was not adequate. How-
ever, Brouwer ('27) determined the projection of the retinal
quadrants on the superior colliculus of the rabbit and found that the lower quadrants are projected to oral and medial
portions and the upper quadrants t o caudal and lateral
regions. He implied that the .superior colliculus is of much higher significance f o r sight in rabbits than in higher mam-
mals arid that it does not serve merely for reflex movements
in these rodents.
Auditory system
The dorsal and ventral cochlear nuclei (fig. 10) are very
prominent in the mole with large numbers of fibers passing by way of the lateral lemniscus to distribute to the inferior colliculus, where, after relay, they distribute by the peduncle of the inferior colliculus to the medial geniculate nucleus of the thalamus.
Stokes ('12) placed the cochlear nuclei medial to the resti-
form body in the opossum but this is not their position in the mole where they occupy positions typical f o r most mammals.
The dorsal cochlear nucleus of this insectivore lies dorsolateral
to the inferior cerebellar peduncle. The fibers arising from this nucleus are both crossed and uncrossed. Some of the fibers curve around the dorsal border of the inferior cerebellar peduncle, others pass through the peduncle ; these fibers then turn ventromediad towards the raph6. Many of them accumu- late in the lateral lemniscus of the same side, which lies at
this level between the genu of the facial nerve dorsally and
the facial nerve and the motor nucleus of that nerve ventrally. The decussating fibers cross the midline dorsal to the g e m of
MIDBRAIN OF THE MOLE 777
servers (as Ariens Kappers, Huber and Crosby, '36) refer to the inferior colliculus as an auditory reflex center which receives auditory impulses and then discharges to the su- perior colliculus and the medial geniculate nucleus, a meta- thalamic auditory center mediating impulses to the cerebral cortex. Mettler ( '32) studied the effects of lesions in the
auditory cortex of cats and stated that it is possible that
certain of the axis cylinders in the brachium of the inferior colliculus do not stop in the medial geniculate bodies but pass
beyond to the cortex. Woollard and Harpman ('40) placed
lesions in the inferior colliculus of guinea pigs and cats and suggested that some fibers pass directly from the inferior colliculus to the cerebral cortex. The present material fur- nished no satisfactory evidence for direct colliculo-cortical fibers.
Spino-tectal tract
The spino-tectal tract occupies a position in the lateral funiculus of the spinal cord adjacent to the spino-thalamic
tract in many mammals. It is impossible to ascertain the
exact position of this pathway in the spinal cord in normal
material. This tract ascends through the spinal cord to enter
the ventrolateral region of the medulla oblongata, a position
which it maintains at lower medullar levels. At such levels in the mole it lies ventromedial to the spino-thalamic tract and to the nucleus of the descending root of the trigeminal.
The spino-tectal tract becomes more distinct as it ascends
through the medulla ventromedial to the nucleus of the de-
scending root of the trigeminal and ventrolateral to the
internal arcuate fibers as they swing into the sensory decus- sation. At the level of the inferior olivary nucleus it lies lateral to this olivary nucleus, ventromedial to the nucleus of the descending root of the trigeminal, and in proximity to the ventral secondary ascending tract of the latter. Cerebello- olivary and olivo-cerebellar fibers passing towards the resti- form body overlie the tract and the external arcuate fibers
are ventral to it along the ventral border of the medulla
775 THOMAS N. J O H N S O N
oblongata. The spino-tectal tract continues its rostral course with the lateral spino-thalamic and ventral secondary ascend- ing tract of the trigeminal, along the dorsolateral portion of the olive, ventromedial to the secondary ascending tract
of the trigeminal. It occupies this position in the ventro-
lateral region of the medulla throughout the level of the
inferior olive. At rostral levels of the medulla it still lies
ventrolateral to the descending root of the trigeminal. At the level of the g e m of the facial nerve and the decussating dorsal cochlear fibers, the spino-tectal tract lies lateral to the superior olivary nucleus, medial to the descending root of the trigeminal, and lateral to the root of the facial nerve
as the latter passes ventrally from the genu (fig. 10). Through
the pons, the medial lemniscus is horizontal in position but
gradually shifts laterad as it ascends so that above the rostral
end of the superior olive it approaches the lateral spino-
thalamic and spino-tectal systems (fig. 8). Fibers of the
lateral lemniscus en route t o^ the^ inferior^ colliculus^ cross
these pathways. At the caudal levels of the superior colliculus the fibers of the spino-tectal tract course dorsad in the lateral
region of the midbrain towards the tectum (figs. 7 and S),
entering its stratum album intermediale. These fibers are mingled with fibers from the ventral secondary ascending tract of^ the trigeniinal in their passage towards the tectum.
At the level of the dorsal tegmental decussation (fig. 6), the
medial lemniscus has turned dorsolateralward with the ventral secondary ascending tract of the trigeminal on its dorsomedial
border. Papez ( '29) placed the spino-tectal tract at the dorsal
tip of the medial lemniscus in the cat. Crosby and Henderson ('48) found that the spino-tectal fascicles form the uppermost
part of the macaque medial lemniscus at upper midbrain
levels and that these fibers of the spino-tectal system swing
in a dorsal direction to enter the superior colliculus external
to the stratum album profundum.
V e n t r a l secondary ascending t r a c t of t h e trigentinal
The trigeminal root in the mole is large, as is t o be ex-
pected since the animal depends to so great an extent upon
780 THOMAS N. JOI-INSON
to enter the tecturn (fig. 6 ) by the intermediate white layer
of the superior colliculus (fig. 5). The main bundles of fibers
then continue forward to the thalamus, medial to the medial lemniscus. Woodburne ( '36) described the trigeminal com- plex in a series of vertebrates and found that in the rabbit
and mouse a small number of fibers of the ventral secondary
ascending tract of the trigeminal enter the tectum of the superior colliculus. Huber et al. ('43) also maintained that collaterals of the ventral secondary ascending tract of the
trigeminal distribute t o the mammalian optic tectum, but
the spino-thalamic and the main fascicles of the ventral secondary ascending tract of the trigeminal terminate di- rectly in the ventral nucleus of the dorsal thalamus.
Cortico-tectcrl systems
Two groups of fibers, the internal and the external cortico- tectal tracts, enter the superior colliculus from the cerebral cortex. Beevor and Horsley ( '02) described occipito-mes- encephalic fascicles in the monkey as composed of large fibers which stand out distinctly from the medium-sized, occipito- thalamic fibers and which pass to the entire extent of the stratum griseum profundum of the superior colliculus. They also demonstrated temporo-mesencephalic fibers in the cat passing primarily from the posterior limb of the ecto-Sylvian gyrus to distribute to the superior colliculus. They did not determine the termination of the latter fibers in the superior colliculus. Crosby and Henderson ( '48) identified external and internal cortico-tectal pathways in the macaque. These
fibers correspond t o the temporo-mesencephalic and occipito-
mesencephalic tracts, respectively, of Beevor and Horsley ('02). Crosby and Henderson traced the external cortico- tectal fibers in their course along the optic pathways; they subdivided the internal system into a dorsal and a ventral division. I n the mole, the internal cortico-tectal fibers from the pre- occipital and occipital areas of the cerebral cortex enter the diencephalon as part of the superior thalamic radiations (fig.
MIDBRAIN OF THE MOLE 781
3) through the internal capsule. Immediately on reaching
the diencephalon the more dorsomedial fibers of the internal capsule are joined by more lateral bundles which swing across the other internal capsule fibers in a dorsomedial direction. Thus a common internal cortico-tectal system is maintained which proceeds dorsocaudalward. Behind the habenula the
fibers pass to the pretectal area (fig. 3 ) , where some may
EXT. CORT. TECT. PRETECT, AREA
Pig. 3 Photomicrograph of a transverse section through the posterior third of the diencephalon of the mole showing the optic tract fibers to the lateral geniculate nucleus and the lateral geniculate nucleus. Ailver preparation. X 30.
synapse, and to the tectum, which they enter by the inter- mediate white stratum (fig. 4). These fibers cannot be traced from their origin in the cerebrum; they can only be demon- strated from the region where they enter the diencephalon to the tectum. The external cortico-tectal fibers enter the diencephalon from the temporal lobe by a sublenticular path and join the
optic tract as it passes dorsally over the cerebral peduncle.
These fibers then pass dorsomedially, external t o the optic
tract, toward the lateral geniculate nucleus where a large nnmber of the optic tract fibers enter this nucleus. Beyond
MIDBRAIN OF T H E MOLE 783
The chief nucleus of the inferior colliculus is directly con- tinuous with the periventridar gray of the superior collicu- lus. The acustico-optic fibers are short, thin, medullated and unmedullated fibers which are found in the nucleus of the inferior colliculus and extend rostralward in the periventricu- lar gray of the superior colliculus to synapse with the den- drites of the periventricular layer. These could not be photographed satisfactorily although they are demonstrable in the material.
E f e r e n t p a t h w a y s from t h e t e c t u m
Medial tecto-spinal, tecto-oculomotor and tecto-rubral s y s t e m s.
The medial tecto-spinal fibers arise from the deep gray
layer of the superior colliculus (fig. 5) and, leaving the tectum
by the stratum album profundum, pass ventrally around the periventricular gray to cross to the opposite side in the dorsal tegmental decussation and then to attain a position ventral to the medial longitudinal fasciculus (fig. 6). Rasmussen ('36), working with cats, produced lesions in the superior and inferior colliculi which caused degeneration of the medial
tecto-spinal tract on the side opposite the lesion but found
no degeneration in the tecto-spinal tract on the side of^ the
lesion below the dorsal tegmental decussation, indicating
that the tract is entirely crossed. He also placed lesions in
the nucleus of the inferior colliculus as far caudally as the
plane of the nucleus of the lateral lemniscus and found no degeneration in the medial tecto-spinal tract. Papez and
Freeman ( '30) reported similar findings i n. the rat. Tsai
('25b), working with the opossum, reported that the tecto- spinal tract (apparently the medial tecto-spinal of the present account) arises from the entire length of the tectum and that
it is both crossed and uncrossed. It is possible that this tract
arises from the entire length of the tectum in different animals
and that it is both crossed and uncrossed in some animals.
After its decussation, the medial tecto-spinal tract passes caudad through the tegmentum of the midbrain and the pons
784 THOMAS N. JOHNSON
in a position ventral to the medial longitudinal fasciculus
(figs. 7 t o 10). I n the caudad portion of the pons, the medial
tecto-spinal tract is found near the midline on each side of the raph6 (fig. 10) and maintains this position in the medulla oblongata to a level through the caudal end of the inferior
olivary nucleus. It assumes a more ventral position when
it reaches the level of the motor decussation. At the upper levels of the spinal cord the tract enters the ventral funiculus medial to the ventral horns and ventral to the medial vestibu-
lar component of the medial longitudinal fasciculus. Its
extent in the cord has not been determined.
Fig. 5 Photomicrograph of a transverse section through the anterior third of the superior colliculi and the medial geniculate nuclei of the mole. The hrachium of the inferior eolliculus should be noted. (^) Weil stain. X 30.
