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Organization of the striatal projections from the rostral caudate nucleus to the globus pallidus the entopeduncular nucleus and the Pars reticulata of the substantia nigra in the cat.

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THE ANATOMICAL RECORD 238114-124 (1994)
Organization of the Striatal Projections From the Rostra1 Caudate
Nucleus to the Globus Pallidus, the Entopeduncular Nucleus, and
the Pars Reticulata of the Substantia Nigra in the Cat
BERNARD0 HONTANILLA, SILVANO DE LAS HERAS, AND JOSfi MANUEL
GIMJ~NEZ-AMAYA
Departamento de Morfologia, Facultad de Medicina, Universidad Autbnoma de Madrid,
Madrid, Spain
ABSTRACT
This study explores the organization of the striatal projections from the rostral caudate nucleus to the output nuclei of the basal
ganglia in the cat. Tracer deposits were stereotaxicallyinjected in different
dorsoventral, mediolateral, and rostrocaudal sectors of the head of the caudate nucleus using horseradish peroxidase (HRP) conjugated with wheat
germ agglutinin (HRP-WGA)either alone or mixed with free HRP. After the
injections, a detailed analysis of the terminal labeling was carried out
within the globus pallidus (GP), the entopeduncular nucleus (Ep), and the
substantia nigra (SN) pars reticulata (SNR). Our findings illustrate how
different dorsoventral, mediolateral, and rostrocaudal parts of the rostral
caudate nucleus project primarily to similarly positioned but spatially segregated parts of GP. The striatoentopeduncular pathway was also organized topographically, but there was overlapping by projections from different parts of the rostral caudate nucleus. Areas of topographical
segregation and zones of overlap were detected in the organization of the
striatal projections from the rostral caudate nucleus to SNR. These results
raise the possibility of distinct striatal actions upon different sectors of the
output nuclei of the basal ganglia and, indirectly, upon their targets in the
thalamus and brainstem. o 1994 WiIey-Liss, Inc.
Key words: Striatum, Caudate nucleus, Striatopallidal projections, Striatoentopeduncular projections, Striatonigral projections, Cat
The basal ganglia form a group of subcortical nuclei
functionally linked with the organization of complicated motor behaviors (Nauta and Feirtag, 1986). They
receive a massive input from the cerebral cortex
through the striatum, the largest structure of the basal
ganglia (Heimer et al., 1985; Parent, 1986; Alheid et
al., 1990; Graybiel, 1990; Gerfen, 1992). From the striatum several pathways reach other basal ganglia nuclei, which project outside these structures (Graybiel
and Ragsdale, 1979; Alexander et al., 1986; Alheid et
al., 1990; Gimenez-Amaya, 1991a,b; Heras et al.,
1993a; Hoover and Strick, 1993). Thus the globus pallidus (GP), the entopeduncular nucleus (Ep), and the
pars reticulata (SNR) of the substantia nigra (SN) receive striatal projections and, in turn, project to different thalamic targets and premotor regions of the brainstem. Internal regulatory loops are also present in the
basal ganglia, most notably the nigrostriatal dopaminergic pathway and the pallidosubthalamic regulatory
loop (Heimer et al., 1985; Parent, 1986; Alheid et al.,
1990).
The hodological organization of the basal ganglia has
been extensively studied over the last 20 years, and we
have a good idea of the connectivity among the different structures involved in their circuits. We still do not
0 1994 WILEY-LISS, INC.
understand, however, the overall organization of the
basal ganglia. A detailed study of striatopallidal, striatoentopeduncular, and striatonigral pathways seems
crucial for this undertaking (Gimenez-Amaya and
Graybiel, 1990, 1991; Gandia and Gimenez-Amaya,
1991; Gimenez-Amaya, 1991a; Graybiel et al., 1991;
Hedreen and DeLong, 1991; Hazrati and Parent,
1992a,b,c; Parent and Hazrati, 1993).
The purpose of the present study was to reveal the
organization of the projections from the rostral caudate
nucleus to GP, Ep, and SNR in the cat. More specifically we sought to determine whether distinct dorsoventral, mediolateral, and rostrocaudal parts of the
rostral caudate nucleus project to comparably positioned parts of GP, Ep, and SNR and whether the projections from separate areas remain spatially segregated. The anterograde transport of horseradish
peroxidase conjugated with wheat germ agglutinin
(HRP-WGA)either alone or mixed with free HRP was
Received April 9, 1993; accepted August 9, 1993.
Address reprint requests to Dr. Jose Manuel Gimenez-Amaya, Departamento de Morfologia, Facultad de Medicina, Universidad Autonoma de Madrid, Ci Arzobispo Morcillo SIN, 28029 Madrid, Spain.
SEGREGATION AND CONVERGENCE OF STRIATAL E F F E R E N T S
115
The histochemical activity of the enzyme acetylcholinesterase (AChE) was revealed by a slightly modified
Geneser-Jensen and Blackstad method (GeneserP
cs 1
F
HRP-WGA 5% + HRP 30%
Jensen and Blackstad, 1971; Graybiel and Ragsdale,
cs 2
F
HRP-WGA 5% + HRP 30%
CN
CS 3A
F
HRP-WGA 5% + HRP 30%
CN 1978) in sections adjacent to those processed for the
CN TMB method.
HRP-WGA 5% + HRP 30%
CS 3B
F
Bright- and darkfield illumination was used to anacs 4
F
HRP-WGA5% + HRP20%
CN
CN lyze the anterograde labeling in sections, which were
cs 5
F
HRP-WGA5% + HRP20%
CN processed for HRP-WGA or HRP-WGMHRP. The sizes
CS 6
F
HRP-WGA 10%
cs 7
F
HRP-WGA 10%
CN of the effective injection sites were estimated by eye
CN and coded in terms of a central zone with the densest
CS 13
M
HRP-WGA 5% + HRP 15%
CS 8l
F
TMB-reaction product and a surrounding zone with a
less intense reaction. The exact location of the antero'Control case for histochemical techniques.
grade labeling in GP, Ep, and SNR was plotted onto
drawings. To delineate the precise limit of the output
nuclei of the basal ganglia, corresponding adjacent
used for these experiments. A preliminary report of AChE sections were used (see Fig. 8C,D). AChE secthis study has been presented previously (GimCnez- tions from case CS 8 helped us to reconstruct the injecAmaya and Hontanilla, 1990).
tion sites in the sagittal and horizontal planes.
TABLE 1. Case number, sex, concentration of tracers,
and location of injection sites
~
MATERIAL AND METHODS
Nine adult cats of both sexes were used for this
study, eight for tracer injections and a n additional one
for histochemistry (Table 1).Before surgery, the animals were deeply anesthetized with sodium pentobarbital (Nembutal) in a proportion of 40 mg/kg i.p. Stereotaxic injections of horseradish peroxidase (HRP)
conjugated with wheat germ agglutinin (HRP-WGA,
5% or 10%) either alone or mixed with free HRP (15%,
20% or 30%) were made into different dorsoventral,
mediolateral, and rostrocaudal parts of the rostral caudate nucleus. Case CS 4 with a massive injection in the
head of the caudate nucleus and case CS 1 with a n
injection of the putamen were used as controls. The
tracer deposits were made with vertically held glass
micropipettes through which brief puffs of air were applied by means of a Picospritzer I1 (General Valve Co.).
Volumes injected ranged from 10-80 nl. In all experiments the atlas of Reinoso-Suarez (1961) was used for
the injections. All cases but CS 3 were injected unilaterally. Case CS 3 was injected bilaterally for a better
comparison of both halves of the brain since there are
no crossed striatopallidal, striatoentopeduncular, or
striatonigral pathways in mammals (Heimer et al.,
1985; Parent, 1986; Alheid et al., 1990).
After a survival period ranging from 44 to 50 h, the
animals were again deeply anesthetized using the anesthetic protocol described above and transcardially
perfused with the following solutions: (1)0.3 1 of saline
(0.9% NaC1); (2) 11 of 1% paraformaldehyde and 1.25%
glutaraldehyde in 0.1 M dibasic phosphate buffer (PB,
pH 7.4); and (3) 0.5 1 of sucrose-PB containing 5% sucrose, 0.5 1 containing 10% sucrose, and 0.5 1 containing
20% sucrose. Next, the brains were removed, blocked,
and soaked overnight at 4°C in a 30% sucrose-PB solution. Finally, they were cut in the coronal plane a t
40-50 pm on a freezing microtome. In case CS 8 we cut
half of the brain on a sagittal plane and the other half
on a horizontal plane.
Sections were processed for HRP-WGA or HRPWGNHRP according to the tetramethyl benzidine
(TMB) protocol of Mesulam (Mesulam, 1978; Mesulam
e t al., 1980), with concentrations of H202ranging from
0.004 to 0.015%. The TMB-series was then counterstained with thionine, dehydrated, and coverslipped.
RESULTS
Deposits of HRP-WGA or HRP-WGAIHRP Into Different
Parts of the Rostra/ Caudate Nucleus
Tracer deposits were made into various parts of the
rostral caudate nucleus to explore systematically the
projections of striatal neurons into the output nuclei of
the basal ganglia. The injections were placed following
the three topographical coordinates: dorsoventral, mediolateral, and rostrocaudal. In this regard, the four
cases shown in Figures 1-8 were chosen to illustrate
the major part of our findings. Thus we tried to inject
into the head of the caudate nucleus at different dorsoventral levels (see cases CS 2 and CS 7 in Figs. 1-4)
and at different mediolateral and rostrocaudal coordinates (see cases CS 3A and CS 3B in Figs. 1 , 2 , 5 , 6 ) . In
cases CS 5, CS 6, and CS 13, the tracer was injected
into medial (CS 5) and dorsal (CS 6 and CS 13)sectors
of the head of the caudate nucleus.
In case CS 2, we injected the dorsal part of the head
of the caudate nucleus in a n intermediate zone following the mediolateral coordinate (Figs. l A , 2C, 3). In
case CS 7, we intended to inject the same rostrocaudal
level as in case CS 2 reaching more ventral portions of
the caudate nucleus (Figs. lB, 2C, 4). These two injections overlapped dorsally and caudally, and the injection of case CS 2 extended over more caudal regions of
the striatum than case CS 7 (Fig. 2C). However, both
injections were well restricted to different dorsoventral
regions of the rostral caudate nucleus and were centered in a precise rostrocaudal region of the striatum
(see the reconstruction of these two injection sites on a
sagittal section of the head of the caudate nucleus in
Fig. 2C).
Figure 2D shows the horizontal reconstruction of the
rostral caudate nucleus with the injection sites of cases
CS 3A (Figs. lC, 2D, 5) and CS 3B (Figs. lD, 2D, 6) and
illustrates the mediolateral and rostrocaudal differences between these tracer deposits. These cases were
injected more caudally than cases CS 2 and CS 7 in the
most medial (case CS 3A) and lateral (case CS 3B)
parts of the rostral caudate nucleus. In case CS 3B, we
attempted to reach the most caudal regions of the head
of the caudate nucleus (Fig. 2D). The injection in case
CS 3B contaminated the internal capsule at some rostrocaudal levels (Fig. 8A).
116
B. HONTANILLA ET AL.
Fig. 1. Photomicrographs in brightfield illumination of four coronal sections illustrating the injection
sites in the rostral caudate nucleus of cases CS 2 (A),CS 7 (B), CS 3A (C), and CS 3B (D).AC, anterior
commissure; IC, internal capsule; LV, lateral ventricle. Scale bar: 1.03 mm.
Anterograde Labeling in GP
All of our injections in the rostral caudate nucleus
elicited conspicuous anterograde labeling in GP, which
was topographically distributed. After the injection in
dorsal and intermediate dorsoventral regions of the
head of the caudate nucleus (see case CS 2 in Figs.
1-31, axonal labeling was found in dorsal and intermediate dorsoventral regions of GP (Fig. 3a-c). This terminal labeling was most conspicuous in the middle
third of GP (Fig. 3b). The anterograde labeling did not
extend prominently to the most ventral portion of this
nucleus at any rostrocaudal level (Fig. 3a-c). In the
middle third, however, some fibers tended to invade the
medial edge of the intermediate dorsoventral region of
GP (Fig. 3b). By contrast, in case CS 7, we observed an
invasion of medial and ventral pallidal areas by labeled axons from more ventral territories in the head of
the caudate nucleus (Fig. 4a-c). At rostral levels of GP,
the anterograde labeling in case CS 7 occupied the subcommissural part of GP (Fig. 4a) and it progressively
innervated the most medial portion of GP in its ventral
sector (Fig. 4b,c).
117
SEGREGATION AND CONVERGENCE OF STRIATAL EFFERENTS
D
R
\
Fig. 2. Sagittal and horizontal schematic reconstructions of the injection sites shown in Figure 1 to illustrate the dorsoventral (A and C)
and mediolateral and rostrocaudal (B and D) location of these tracer
deposits. In C, cases CS 2 and CS 7 are drawn over the schema of a
sagittal section from case CS 8 and stained for AChE as illustrated
above (A). Note the dorsoventral territories in the striatum covered by
those injections, the overlap between them, and the heterogeneous
distribution of this enzyme within the striatal tissue, leaving areas
with more and less AChE, notably in the rostral part of the caudate
nucleus. In D, cases CS 3A and CS 3B are drawn over the schema of
a horizontal section also from case CS 8 and stained for AChE as
illustrated above (B). Note the mediolateral and rostrocaudal territories of the striatum involved with these injections. AC, anterior commissure; D, dorsal; IC, internal capsule; LV, lateral ventricle; M, medial; R, rostral; T, thalamus. Scale bar: A, 1.15 mm; B, 1.23 mm.
The evaluation of the topographical variations of anterograde labeling in GP following the mediolateral
and rostrocaudal coordinates is illustrated with the bilateral HRP-WGA/HRP striatal injections of animal
CS 3. In case CS 3A, after a medial and intermediate
dorsoventral injection in the rostral caudate nucleus,
labeled axons were found in the most medial regions of
all the rostrocaudal parts of the middle third of GP
(Fig. 5a-c). In sharp contrast, in case CS 3B with a
more lateral, dorsal, and caudal injection in the head of
the caudate nucleus, the labeling in GP was confined to
the dorsal half of the middle rostrocaudal third (Figs.
6b, 8A), and to the dorsal and middle dorsoventral sectors of the caudal third (Fig. 6c).
B. HONTANILLA ET AL.
118
cs 7
cs 2
u
L M
a
D
b
C
a
d
e
b
C
f
Fig. 3. At the top, schematic drawings of two coronal sections at
different rostrocaudal levels of the head of the caudate nucleus with
the center of the injection site in case CS 2. At the bottom, schematic
drawings of three rostrocaudal levels of GP (a+) and Ep (d-fl showing the anterograde labeling found in these structures after this striatal injection. AC, anterior commissure; Acc, accumbens nucleus; C1,
claustrum; CN, caudate nucleus; D, dorsal; Ep, entopeduncular nucleus; GP, globus pallidus; LV, lateral ventricle; M, medial; P, putamen.
Anterograde Labeling in Ep
The anterograde labeling in Ep was evaluated following the same topographical coordinates studied for
the striatopallidal pathway (Fig. 2). Thus regarding
the dorsoventral coordinate, cases CS 2 and CS 7
showed terminal labeling in all rostrocaudal levels of
Ep after tracer injections in the dorsal and more ventral striatal territories of the head of the caudate nucleus (Figs. 1-4). The labeling was fairly segregated in
the rostral and middle rostrocaudal thirds of Ep (compare Figs. 3d-e, 4d-e). In case CS 2, the rostral innervation of Ep was confined to the intermediate mediolateral region (Fig. 3d). In contrast, the injection in
case CS 7 elicited anterograde labeling in medial regions in the rostral and middle rostrocaudal thirds of
Ep (Fig. 4d-e). In both cases, the terminal labeling
from the rostral caudate nucleus was localized in medial regions of the caudal third of Ep (Figs. 3f, 4f).
The organization of the striatoentopeduncular pathway following the mediolateral and rostrocaudal coordinates was analyzed in cases CS 3A and CS 3B. Only
d
e
'
f
Fig. 4. At the top, schematic drawings of two coronal sections from
case CS 7 at different rostrocaudal levels of the head of the caudate
nucleus with the center of the injection site. At the bottom, schematic
drawings of three rostrocaudal levels of GP ( a 4and E p (d-0 showing the anterograde labeling found in these structures after this striatal injection. AC, anterior commissure; CN, caudate nucleus; D, dorsal; Ep, entopeduncular nucleus; GP, globus pallidus; LV, lateral
ventricle; M, medial.
the rostral and medial injection of case CS 3A labeled
the rostral third of Ep (Figs. 5d, 6d). These two cases
showed fairly well segregated labeling in the middle
rostrocaudal third of Ep (Figs. 5e, 6e). However, the
injection in case CS 3A labeled scattered terminals in
lateral territories of Ep (Figs. 5e, 8B), which overlapped the anterograde labeling produced by the caudal, lateral, and dorsal injection in the head of the caudate nucleus of case CS 3B (Fig. 6e).
Anterograde Labeling in SNR
The anterograde labeling in SN is shown in Figure 7
for all cases with topographical injections into the head
of the caudate nucleus (Figs. 1,2).Since our description
is focused on striatal connections from the rostral caudate nucleus to the output nuclei of the basal ganglia,
the anterograde labeling elicited in SNR is described in
detail.
Dorsal injections in the rostral caudate nucleus elicited anterograde labeling that invaded ventral parts of
the rostral SNR (for this dorsoventral topographical
119
SEGREGATION AND CONVERGENCE OF STRIATAL EFFERENTS
cs 3 A
CS 3B
\
An
u
L,
A
a
a
b
e
C
C
d
d
b
f
Fig. 5. At the top, schematic drawings of two coronal sections from
case CS 3A at different rostrocaudal levels of the head of the caudate
nucleus with the center of the injection site. At the bottom, schematic
drawings of three rostrocaudal levels of GP (ax)and Ep (d-f) showing the anterograde labeling found in these structures after this striatal injection. AC, anterior commissure; C1, claustrum; CN, caudate
nucleus; D, dorsal; Ep, entopeduncular nucleus; GP, globus pallidus;
IC, internal capsule; M, medial; P, putamen.
inversion of the striatonigral pathway compare corresponding sections a of cases CS 2 and CS 7, and corresponding sections a and b of cases CS 3A and CS 3B in
Fig. 7). Moreover, when all the striatal injections are
considered (see cases CS 2, CS 7, CS 3A, and CS 3B in
Fig. 7), it can be seen that the axonal labeling they
elicited partially overlapped a t the level of the intermediate mediolateral third of the rostral half of SNR.
However, other SNR regions did not receive projections from all of the striatal sectors injected. This was
the case, for instance, in the most medial aspects of
SNR. In these mesencephalic regions, the tracer injection of case CS 3B did not produce labeling throughout
the rostrocaudal extension of SNR (see case CS 3B in
Fig. 7). Some medially extending fibers were only
found in caudal regions of SN (see the corresponding
section d of case CS 3B in Fig. 7).
In general, the anterograde labeling in the rostral
half of SNR of the two pairs of cases considered (Fig. 2)
was localized medially or laterally (see corresponding
sections a and b of the four cases in Fig. 7). Thus the
e
f
Fig. 6. At the top, schematic drawings of two coronal sections from
case CS 3B at different rostrocaudal levels of the head of the caudate
nucleus with the center of the injection site. At the bottom, schematic
drawings of three rostrocaudal levels of GP (a-c)and Ep (d-f) showing the anterograde labeling found in these structures after this striatal injection. CN, caudate nucleus; D, dorsal; Ep, entopeduncular
nucleus; GP, globus pallidus; IC, internal capsule; LV, lateral ventricle; M, medial; P, putamen.
axons labeled by rostral injections t h a t reached dorsal
and ventral striatal territories in the rostral caudate
nucleus innervated medial territories in the rostral
half of SNR (see corresponding sections a and b of cases
CS 2 and CS 7 in Fig. 7). More caudally, labeled axons
in both cases innervated more lateral territories of
SNR (see corresponding sections c and d of cases CS 2
and CS 7 in Fig. 7; see also Fig. 8D for case CS 2).
Striatal injections that reached more caudal areas of
the lateral and medial regions of the head of the caudate nucleus elicited labeling in more lateral portions
of the rostral half of SNR (see corresponding sections a
and b in cases CS 3A and CS 3B of Fig. 7). However, in
case CS 3A, some labeling was observed medially
throughout the rostrocaudal extension of SNR (see corresponding sections a 4 of case CS 3A in Fig. 7). Labeled axons were also scattered in the medial part of
SN in the caudal section of case CS 3B (see the corresponding section d for case CS 3B in Fig. 7). All of the
injected striatal regions projected to the most caudal
portions of SN (see corresponding sections d of the four
cases in Fig. 7).
120
B. HONTANILLA ET AL.
cs 2
cs 7
CS 3A
A
Fig. 7. Schematic drawings of four rostrocaudal sections of SN in cases CS 2, CS 7, CS 3A, and CS 3B,
illustrating the anterograde labeling in this mesencephalic structure after injections in the rostral
caudate nucleus. To simplify the figure, sections have been marked from rostral (a) to caudal (d)only on
the left side of case CS 2. A8, retrorubral area; CP, cerebral peduncle; D, dorsal; M, medial; SNC,
substantia nigra, pars compacta; SNL, substantia nigra, pars lateralis; SNR, substantia nigra, pars
reticulata.
Heterogeneous Distribution of Anterograde Labeling in
Ep, and SNR
GP, Parent, 1986; Gandia and Gimenez-Amaya, 1991;
The organization of the anterograde striatal labeling
in the output nuclei of the basal ganglia was heterogeneous. Thus some areas of these nuclei were more labeled than others, and within these more intensely labeled areas it was possible to detect zones of intense
and conspicuous labeling intermingled with areas of
lighter labeling. These findings, although observed in
GP and Ep (Figs. 3-6,8A,B), were clearer seen in SNR
after the tracer injections in the rostral caudate nucleus. Figure 7 illustrates these neuroanatomical observations throughout the entire rostrocaudal extension of SN (see also Fig. 8D for case CS 2).
DISCUSSION
Methodological Considerations
The use of HRP-WGA as an anterograde tracer has
been extensively discussed in the literature. Our own
experiments and the results of others have shown that
HRP-WGA is a good anterograde tracer, and it has
been used previously to determine the neuroanatomical organization of the efferent connectivity of the striatum in mammals (Royce and Laine, 1984; Smith and
Gimenez-Amaya and Graybiel, 1991; Hedreen and DeLong, 1991; Gandia, 1992). Moreover, orthograde tracing evaluation of the striatopallidal, striatoentopeduncular and striatonigral pathways does not present the
fiber-of-passageproblem, as might be the case for other
projections within the basal ganglia themselves (Gandia, 1992). Nevertheless, some methodological problems need to be mentioned.
First, it is important to note that some of the labeling
observed in GP might represent striatal fibers coursing
to Ep and SN. Similarly, labeling in Ep might represent striatal projections to SN. Therefore, the actual
terminal labeling in GP and/or Ep might be less abundant than described in our results. Moreover, striatonigral fibers that penetrated the capsular margin of GP
(striatal projections from the head of the caudate nucleus) and Ep could also explain the heterogeneous distribution of the anterograde labeling in GP and Ep.
Although we have minimized this problem for almost
all of GP and for the ventral part of Ep, we cannot rule
out the possibility that some of the anterograde labeling evaluated as terminals in the capsular margin of
GP and in Ep might actually be striatonigral fibers
SEGREGATION AND CONVERGENCE OF STRIATAL EFFERENTS
121
Fig. 8. Photomicrographs illustrating examples of anterograde labeling in the three output nuclei of the basal ganglia after different
topographical injections in the head of the caudate nucleus. A Darkfield photomicrograph showing the caudal area of the injection site in
the caudate nucleus and terminal labeling in dorsal portions of GP of
case CS 3B. B: Darkfield photomicrograph illustrating anterograde
labeling in Ep in case CS 3A. C and D Pair of adjacent sections
illustrating anterograde labeling in SN (D) and the corresponding
AChE (C) in case CS 2. CN, caudate nucleus; Ep, entopeduncular
nucleus; GP, globus pallidus; IC, internal capsule; MRF, mesencephalic reticular formation; PGM, periaqueductal gray matter; SNC, substantia nigra, pars compacta; SNL, substantia nigra, pars lateralis;
SNR, substantia nigra, pars reticulata; T, thalamus. Scale bar: A,
0.87 mm; B, 0.78 mm; C and D, 0.93 mm.
running through those nuclei. However, the observations discussed here are quite similar to those reported
by Royce and Laine (1984) using tritiated aminoacid
3H-proline autoradiography.
Second, the limited capsular involvement in case CS
3B might indicate the presence of striatal fibers from
other portions of the caudate nucleus. As the worst
possibility, we might have contaminated more rostral
regions of the lateral and dorsal portions of the caudate
nucleus and never reached the rostrocaudal level of
case CS 3A. Even this, however, would not invalidate
our evaluation of the rostrocaudal topographical preservation of the striatal output from the rostral caudate
nucleus in the cat.
Another interesting possibility is the double or triple
branching by the striatal fibers that extend from the
122
B. HONTANILLA ET AL.
head of the caudate nucleus to the output nuclei of the
basal ganglia. In this hypothetical case, the striatal
fibers that innervate GP might also reach Ep and even
terminate in SN. This would not modify our interpretation of the results and would even enrich them substantially. Nevertheless, the studies of Beckstead and
Cruz (1986) in the cat have shown that the striatal
axons that innervate GP, Ep, and SN come from different cell populations within the caudate nucleus (see
also Koliatsos et al., 1988, Parent et al., 1989;
Gimenez-Amaya and Graybiel, 1990; Selemon and
Goldman-Rakic, 1990; Gimenez-Amaya and Graybiel,
1991).
Topographical Preservation vs. Segregation and
Convergence of the Striatal Efferents From the Rostra1
Caudate Nucleus
Our results show a topographical preservation of the
dorsoventral, mediolateral and rostrocaudal coordinates in the striatopallidal pathway. Although there
were some pallidal areas showing a small degree of
convergence by projections from different sectors of the
rostral caudate nucleus, GP receives topographically
organized projections from the head of the caudate nucleus. These observations agree with those of previous
studies in the cat (Niimi et al., 1970; Usunoff et al.,
1974; Royce and Laine, 1984), rat (see references in
Heimer et al., 1985; Gandia and Gimenez-Amaya,
1991; Gandia, 1992), and primate (see references in
Royce and Laine, 1984; Parent, 1986; Alheid et al.,
1990; Hedreen and DeLong, 1991; see also Hazrati and
Parent, 199213; Parent and Hazrati, 1993). Since GP is
topographically linked with the reticular thalamic nucleus (Nauta, 1979; Haber et al., 1985; Parent et al.,
1988; Cornwall et al., 1990; Hazrati and Parent, 1991;
Gandia et al., 1993; Heras et al., 1993a), the striatopallidal pathway might innervate distinct populations
of pallidal cells that project to different parts of the
reticular thalamic nucleus depending on the striatal
sector under consideration. Thus the striatopallidal
pathway could regulate the flow of different thalamocortical and corticothalamic fibers (Jones, 1975, 1985;
Yen et al., 1985; Gandia et al., 1993; Heras et al.,
1993a).
Regarding the organization of the striatoentopeduncular pathway, our results reflect the topographical
preservation in the three coordinates under study, but
there is more overlapping than in GP. The mediolateral
and rostrocaudal organization of this pathway was
fairly well segregated in Ep. However, some sectors
overlapped, most notably in the lateral portions of Ep
(see cases CS 3A and CS 3B in Figs. 5e, 6e) and in the
medial areas of the caudal Ep (see cases CS 2, CS 7 and
CS 3A in Figs. 3f, 4f, 5f). Furthermore, the dorsoventral organization of this pathway was not as clearly
segregated as in the striatopallidal projections. Interestingly, when two striatal sectors in the head of the
caudate nucleus that were far away from each other
were considered simultaneously, it could be seen that
their projections to Ep preserved the dorsoventral, mediolateral, and rostrocaudal coordinates (compare cases
CS 7 and CS 3B in Figs. 4 and 6). This organization of
the striatoentopeduncular pathway might have functional consequences in the outflow of Ep to the thalamus and brainstem (Graybiel and Ragsdale, 1979;
Hendry et al., 1979; Nauta, 1979). Thus different striatal sectors in the rostral caudate nucleus might influence, together or separately, specific areas of the thalamus and brainstem through their innervation of Ep.
SNR is the output nucleus of the basal ganglia that
has a major degree of convergence in the projections
from the head of the caudate nucleus. Our results are in
good agreement with those from previous studies in that
the caudate nucleus projects abundantly to SNR (see
references in Royce and Laine, 1984). We have also
confirmed the results of Royce and Laine (1984) showing projections from the head of the caudate nucleus to
the entire rostrocaudal length of SNR. Evaluating the
topographical arrangement of these projections was
more difficult, and this seems to be the case in other
mammalian species as well (see Hedreen and DeLong,
1991, in the primate; and Gandia, 1992; Heras et al.,
199313, in the rat). Our study illustrates, however, the
need for a more detailed evaluation of the topographical
ordering of the striatonigral pathway in specific rostrocaudal sectors of SNR. In this context, more topographical correspondencesin the striatal projections from the
rostral caudate nucleus to SNR might be found (see for
the organization of the striatonigral pathway in the rat,
Gerfen, 1985;Gandia, 1992; Gerfen, 1992).Overall, our
findings show that SNR was the output nucleus of the
basal ganglia where most striatal sectors of the rostral
caudate nucleus projected in a converging fashion. This
finding is very suggestive regarding the abundant connectivity of SNR with the thalamus (Kultas-Ilinsky et
al., 1978;Hendry et al., 1979; Beckstead, 1983; Takada
et al., 1984; Ilinsky et al., 1987; Kemel et al., 1988;
Cornwall et al., 1990; Pare et al., 1990; Gandia et al.,
19931, superior colliculus (Graybiel, 1978; Harting et
al., 19881, and brainstem (Graybiel and Ragsdale, 1979;
Parent, 1986; Alheid et al., 1990).
In conclusion, our results appear to support the very
recent hypothesis of Parent and Hazrati (19931, which
notes that neither the view of the basal ganglia being
linked with the cerebral cortex through multiple, functionally segregated, parallel circuits (Alexander et al.,
1986; Alexander and Crutcher, 19901, nor the conclusion drawn from Golgi studies of there being a high
degree of convergence by functionally distinct inputs
within the striatal output (Percheron et al., 1984;
Percheron and Filion, 1991) is entirely true. It seems
more probable that the striatum has multiple representations in the three output nuclei of the basal ganglia (Gandia and Gimenez-Amaya, 1991; GimenezAmaya, 1991a; Hazrati and Parent, 1992b; Parent and
Hazrati, 1993).
Functional Observations
Our results illustrate a topographical preservation of
striatal projections from the rostral caudate nucleus to
GP. This nucleus conspicuouslyprojects to the reticular
thalamic nucleus. These two facts enable us to speculate that the pallidoreticular projection conveys very
specific striatal information. Thus striatal sectors related very specifically with the cerebral cortex (see references in Parent, 1986; Alheid et al., 1990) could effectively influence the thalamic flow with the cerebral
cortex through the gabaergic cells in the reticular thalamic nucleus. In short, the reticular thalamic cells
might or might not inhibit the corticothalamic and
SEGREGATION AND CONVERGENCE OF STRIATAL EFFERENTS
123
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her help with the photographs, and C.F. Warren for
Efferent connections of the ventral uallidum: Evidence of a dual
improving the English. This study was supported by
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