Efferent connexions of the pars lateralHs of the substantia nigra (SNL)
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J. Anat. (1979), 129, 2, pp. 405-412 405
With 5 figures
Printed in Great Britain
Efferent connexions of the pars lateralHs of the
substantia nigra (SNL)
W. W. KAELBER* AND A. K. AFIFI
Departments of Anatomy and Neurology, College of Medicine,
Uniiversity of Iowa, Iowa City, Iowa 52242, U.S.A., and the
Department of Human Morphology, American University of Beirut,
School of Medicine, Beirut, Lebanon
(Accepted 22 August 1978)
INTRODUCTION
The pars lateralis of the substantia nigra (SNL) in the cat was described by Ingram,
Hannett & Ranson (1932). While several studies are available in the literature on
the efferent connexions of the pars compacta (SNC) and pars reticularis (SNR) of
the substantia nigra in cats (Carpenter & McMasters, 1964; Cole, Nauta & Mehler,
1964; Afifi & Kaelber, 1965; Moore, Bhatnager & Heller, 1971; Maler, Fibiger &
McGeer, 1973; Kultas-Llinsky et al. 1977), no data are available on the connexions
of the pars lateralis. The purpose of this study was to determine whether the SNL
projects to the same or different sites as those described for the pars compacta and
reticularis.
MATERIALS AND METHODS
Ten cats were used. Unilateral lesions were placed in the SNL in eight, and the
pars compacta and reticularis in two, using the stereotaxic co-ordinates of Jasper &
Ajmone-Marsan (1953) in a slightly modified form. In all animals the substantia
nigra was approached through the vertical plane using 26 gauge monopolar nichrome
electrodes insulated except for 0)25 mm at the tip. The lesions were produced by a
direct current of 2 mA applied for 5-10 seconds. Animals were killed 10 days post-
operatively under anaesthesia. The brains were perfused with normal saline followed
by 10 % formalin buffered with sodium cacodylate. They were then further fixed for
at least 2 weeks in buffered 10 % formalin. Frozen serial sections were cut in the
transverse plane. Two sections cut at 30 ,um were stained by the modified Fink-
Heimer (1967) and De Olmos-Ingram (1971) silver methods for degenerating axons
and terminals; adjacent 60 ,m thick sections were stained by the Weil and cresyl
violet methods for orientation purposes.
RESULTS
In six animals the bulk of the SNL was destroyed without encroaching on the
cerebral peduncle (Fig. 1). In two other animals the lesion also extended slightly
into the underlying cerebral peduncle. The electrode track in the eight animals
passed through the suprasylvian gyrus, pulvinar and/or the posterolateral nucleus
* Reprint requests to Dr W.W. Kaelber, University of Iowa.
0021-8782/79/2828-6500 $02.00 © 1979 Anat. Soc. G.B. & I.406 W. W. KAELBER AND A. K. AFIFI
Fig. 1. Photomicrograph of the mid-brain showing the electrolytic lesion in the pars lateralis
of the substantia nigra. Cresyl violet. x 8-7.
of the thalamus, medial geniculate body and medial lemniscus. The stria terminalis
and hippocampus were not damaged.
In one additional animal parts of the SNC and SNR were destroyed and the
lesion infringed upon the cerebral peduncle. In another animal, the lesion was in
the SNC and encroached upon the cerebral peduncle. The electrode tracks in these
two animals passed through the medial suprasylvian gyrus, the posterolateral and
ventromedial thalamic nuclei, the medial lemniscus and the central tegmental tract.
In cats with SNL lesions, degenerating fibres and/or terminals were seen in the
following structures: pars compacta and pars reticularis of the substantia nigra
(Fig. 2), homolateral and contralateral superior colliculi, homolateral inferior col-
liculus, periaqueductal gray, pretectal region, posterior commissure, medial reticular
formation, central tegmental tract (CTT), red nucleus, subthalamic nucleus, medial
geniculate body, medial lemniscus, head of the caudate nucleus, putamen, central
(CAN) and lateral (LAN) amygdaloid nuclei (Fig. 3), ventral anterior nucleus of
the thalamus (VA), ventral lateral nucleus of the thalamus (VL), ventral postero-
lateral (VPL) and posteromedial nuclei (VPM) of the thalamus, posterolateral
nucleus of the thalamus (LP), and pulvinar.
The degenerating fibres and terminals in the head of the caudate nucleus were
limited to a zone in the dorsolateral third of the nucleus. The degeneration and
terminals were scanty in VL as compared to VA. The degenerating fibres and
terminals in LAN were more abundant than in CAN.
In cats with SNR and/or SNC lesions, degenerating fibres and terminals wereConnexions of substantia nigra 407
"
% ., . I h 2i. *
Fig. 2. Photomicrograph of abundant fibre degeneration and terminals within the pars compacta
of the substantia nigra. De Olmos-Ingram. x 350.
seen in both superior colliculi, the red nucleus, periaqueductal gray, pretectal region,
subthalamic nucleus, caudate nucleus, and the VA and VL nuclei of the thalamus
in addition to the VPL and VPM and the CTT. No degeneration, however, was seen
in the amygdaloid nuclei of these animals.
DISCUSSION
The different sites of degenerating fibres and terminals reported in this study can
be grouped into three categories: (I) degeneration due to the electrode track;
(2) degeneration due to interruption of fibres of passage within SNL; and (3) true
degeneration resulting from damage to the SNL cell bodies.
The first group includes degeneration observed in the following sites: medial
geniculate nucleus, LP, VPM, and VPL, medial lemniscus, pulvinar, and the CTT
(in animals with lesions in SNC and SNR). In all these the electrode track either
passed through the nucleus or through a neural tract that projects to it.
The second category includes degeneration observed in the superior colliculus,
inferior colliculus, red nucleus, subthalamic nucleus, pretectal area and periaque-
ductal gray matter. Earlier studies (Carpenter & McMasters, 1964; Cole et al. 1964;
Afifi & Kaelber, 1965) described degenerating fibres and terminals in the above
locations as emanating from the substantia nigra. In a later investigation (Afifi,
Bahuth & Jabbur, 1970), using anterograde and retrograde degeneration techniques,408 W. W. KAELBER AND A. K. AFIFI
t.~~~~~~~~~~~~~~~~~ ~~~~~~~~~ .: . . . . . . g ::
Fig. 3. Photomicrograph of fibre degeneration and terminals in the lateral amygdaloid nucleus.
De Olmos-Ingram. x 350.
the origin of the nigrotectal tract was shown to be the cerebral cortex rather than
the substantia nigra. In another study (Afifi, Bahuth & Muffarij, 1970) using antero-
grade and retrograde degeneration techniques, the origin of the nigrorubral and
nigrosubthalamic tracts was similarly shown to the cerebral cortex. In a series of
unpublished experiments we have recently shown that the degenerating fibres and
terminals previously described in the inferior colliculus, pretectal area and peri-
aqueductal gray after nigral lesions (Carpenter & McMasters, 1964; Cole et al. 1964;
Afifi & Kaelber, 1965) actually originate in the cerebral cortex. In all the above
studies, anterograde degeneration was sought, using Nauta and Fink-Heimer
methods with survival periods varying from 7 to 14 days. Similarly, retrograde
degeneration in the substantia nigra was looked for after survival periods of 7-32
days. The identity of the course of degenerating fibres and terminals in all these
sites following nigral and motor cortex lesions, and the absence of retrograde
degeneration in the nigra after lesions in these sites even after 32 days, make us believe
that the previously reported degenerating fibres and terminals in all these sites
following nigral lesions were really due to interruption of fibres of passage through
the nigra. Studies are in progress in our laboratory to confirm these conclusions
using radioactive amino acid injection into the substantia nigra followed by radio-
autography.
The third group, comprising true efferents from the SNL, include the caudate,
putamen, medial reticular formation, CTT, SNC and SNR, amygdala, ventralConnexions of substantia nigra 409
anterior and ventral lateral thalamic nuclei. Figures 4 and 5 are composite diagrams
of these connexions.
Projections from the SNL to the striatum and thalamus deserve some comment.
Those to the caudate are limited to the dorsolateral third of the head of the caudate
nucleus and are abundant compared to those seen in the thalamus.
In contrast, projections from the SNC and SNR are more abundant in the thalamus
and scanty in the caudate. SNL projection to the thalamus is mainly to VA. SNC
and SNR, on the other hand, project equally to VA and VL. These findings may
suggest a preferential projection of the SNL to the striatum and VA, and of SNC-
SNR to the thalamus.
Projections to the medial reticular formation of the mid-brain are also seen
/A/ NCP MG
VLRe
N2m
(2 En ~~~~~~~CAN
NA
A
..-N N
5
Figs 4 and 5. Composite schematic diagrams to show efferent projections from the pars lateralis
of the substantia nigra. (See pp. 411-412 for abbreviations).410 W. W. KAELBER AND A. K. AFIFI
preferentially in animals with SNL lesions as compared to those in SNC and SNR.
Physiological studies by York (1972) suggest that nigral projection to the reticular
formation is part of a system contributing facilitatory influences to the spinal cord
via the reticulospinal tract.
The nigro-amygdaloid connexions, to our knowledge, have only been described
in one study (Kaelber & Afifi, 1977). There are no studies available which compare
the efferent connexions of the SNL with those of the SNC and SNR. In none of the
available studies on substantia nigra (Carpenter & McMasters, 1964; Cole et al.
1964; Afifi & Kaelber, 1964; Moore et al. 1971; Maler et al. 1973; Kultas-Llinsky
et al. 1977) was the SNL involved in the lesion. Fox (1940) describes fibres of unknown
origin reaching the amygdala via the external capsule in a manner similar to those
observed in this study. Terminals in the amygdaloid body are more abundant in
LAN than CAN. Hall (1972) proposes that the most lateral part of CAN is a tran-
sitional zone between CAN and the putamen that provides a bridge between the
amygdala proper and the extrapyramidal system. It is thus conceivable that LAN
and CAN represent sites through which the substantia nigra may exert influence
upon extrapyramidal motor activity.
Degenerating fibres in the CTT were seen in animals with SNL lesions as well as
those with SNC-SNR lesions. The degenerations in CTT in the latter are attributed
to the passage of the electrode track through CTT. Although CTT was not directly
involved by the electrode track or the electrolytic lesion in the SNL animals, it is con-
ceivable that CTT fibres were nevertheless indirectly damaged by virtue of their
proximity to the electrode track or lesion. Further studies are obviously needed to
insure that SNL is the source of such CTT degenerations.
The degeneration and terminals seen in the SNC-SNR after SNL lesions suggest
intrinsic connexions between these different zones of the nigra. Similar intrinsic con-
nexions have been described after discrete lesions in SNC and SNR (Afifi & Kaelber,
1965).
The present study therefore suggests that (1) while the SNL shares some of the
classical connexions described for SNC-SNR, it does have its own connexions to the
amygdala, medial reticular formation and the CTT, and (2) there is a specialization
within different zones of the substantia nigra such that the SNC-SNR areas project pre-
dominantly to the thalamus while the SNL projects primarily to the striatum and VA.
Support for the concept of nigral specializations has come recently from the
work by Kultas-Llinsky et al. (1977) who found differential projection of different
parts within SNR to the striatum and thalamus.
SUMMARY
Unilateral lesions were made in the lateral nucleus of the substantia nigra in eight
cats and in the zona compacta and reticularis in two cats. After a 10 days survival
period, brains were perfused and stored in 10 % formalin. Frozen sections were stained
with the De Olmos-Ingram and Fink-Heimer silver methods for degenerating axons
and terminals. Efferents from the lateral nucleus of the substantia nigra projected
to the dorsolateral third of the head of the caudate nucleus, putamen, medial reticular
formation, central tegmental tract, amygdala, zona compacta and reticularis of the
substantia nigra, ventral anterior and ventral lateral thalamic nuclei. Projections
to the amygdala, medial reticular formation and central tegmental tract were seen
only in animals with lesions in the lateral nucleus of the substantia nigra. ProjectionsConnexions of substantia nigra 411
to the caudate and putamen were more abundant when compared to those in the
thalamus. Within the thalamus, projections to the ventral lateral nucleus were scanty
compared to those in the ventral anterior nucleus. The present study compares for
the first time efferent connexions of the lateral nucleus of the substantia nigra and
those of the pars compacta and reticularis. The findings suggest a specialization of
the different zones of the substantia nigra with regard to their projection sites.
This study was supported in part by USPHS grant GM23336 and grants from the
American University of Beirut School of Medicine Research Fund and the Lebanese
Council for Scientific Research. The technical assistance of Mrs Janice Schafer is
greatly appreciated.
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ABBREVIATIONS
A V, Nucleus anterior ventralis EN, Entopeduncular nucleus
BAN, Basal amygdaloid nucleus Fil, Nucleus filiformis
C, Substantia nigra, pars compacta Fx, Fornix
CAN, Central amygdaloid nucleus Gp, Globus pallidus
CC, Corpus callosum IC, Internal capsule
Cd, Caudate nucleus L, Substantia nigra, pars lateralis
CL, Nucleus centralis lateralis LAN, Lateral amygdaloid nucleus
Cl, Claustrum LD, Nucleus lateralis dorsalis
CoAN, Cortical amygdaloid nucleus LG, Lateral geniculate
CP, Cerebral peduncle LP, Nucleus lateralis posterior
CTT, Central tegmental tract MAN, Medial amygdaloid nucleus
EC, External capsule MD, Nucleus medialis dorsalis412 W. W. KAELBER AND A. K. AFIFI
MG, Medial geniculate Rh, Nucleus rhomboidalis
ML, Medial lemniscus RN, Red nucleus
NCM, Nucleus centralis medialis S, Stria medullaris
NCP, Nucleus of posterior commissure Sg, Nucleus suprageniculatus
OT, Optic tract St, Stria terminalis
PC, Posterior commissure V, Ventricle
Prt, Pretectal area VA, Nucleus ventralis anterior
Pu, Putamen VL, Nucleus ventralis lateralis
Pul, Pulvinar VM, Nucleus ventralis medialis
R, Substantia nigra, pars reticularis VPL, Nucleus ventralis posterolateralis
Re, Nucleus reuniens III, Oculomotor nerve
Ret, Reticular nucleusYou can also read
