Download The visual-oculomotor striatum of the cat: functional relationship to

Exp Brain Res (2001) 136:138–142
DOI 10.1007/s002210000606
RESEARCH NOTE
John K. Harting · Bruce V. Updyke
David P. Van Lieshout
The visual-oculomotor striatum of the cat:
functional relationship to the superior colliculus
Received: 31 August 2000 / Accepted: 4 October 2000 / Published online: 10 November 2000
© Springer-Verlag 2000
Abstract The visual-recipient sector of the cat striatum
receives corticostriate input from over 15 higher visual
and oculomotor-related areas of the cortex and appears
homologous with the physiologically characterized region of mixed visual and oculomotor inputs within the
primate caudate nucleus. This area in the cat involves the
dorsolateral caudate and a strip of the caudal putamen. In
a first series of experiments, the former was injected
with a retrograde tracer in several cats. Thalamostriate
cells were found in extensive regions, including the intralaminar nuclei, certain motor-related nuclei, and, most
notably, across much of the extrageniculate visual thalamus. In another set of experiments, anterograde tracers
were also injected into the superior colliculus (SC), and
labeled tectothalamic fibers were observed in all thalamic sites projecting to the visual-recipient striatum. These
findings highlight for the first time the need for the SC to
be considered in models of thalamostriate and visual/
oculomotor-striatal function(s). Moreover, the data bring
to light the fact that basal-ganglia outflow reaching the
SC via striatonigro-nigrotectal circuitry is well positioned to modulate ascending tecto-thalamic-thalamostriatal signals destined for the visual-recipient striatum.
Keywords Striatum · Superior colliculus · Thalamus
striate projections in the regulation of saccades is poorly
defined. The current findings are novel in revealing a
relatively widespread thalamostriate input to the visualrecipient striatum and, most important, the innervation of
these extensive projections by the superior colliculus.
Materials and methods
All surgical procedures were carried out in accordance with the
National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH publication 80–23, revised 1978). All cats
were anesthetized with sodium pentobarbital (38 mg/kg, ip). In
several cats, 0.03–0.125 µl of 1.25–1.5% wheat-germ agglutinin
conjugated to horseradish peroxidase (WGA-HRP; Sigma) dissolved in saline was injected into the visual-recipient region of the
caudate nucleus, identified by Updyke (1993). In several other
cats, the same tracer was injected into the superior colliculus. Following all injections, the surgical opening was cleaned, the dura
drawn back over the exposed brain, the bone flap replaced, the
surgical opening closed, and antibiotics administered. Animals
were monitored post-operatively and administered analgesics.
Postoperative survivals were 40–50 h, after which the cats
were killed with an overdose of sodium pentobarbital and perfused
with buffered saline followed with 2 l of 0.5% paraformaldehyde–2.5% glutaraldehyde in 0.1-M phosphate buffer, at pH 7.4,
and a post-fix rinse consisting of 1 l of 0.1-M phosphate buffer
containing 5% sucrose. The brains were later sectioned at 40 µm,
after which a one in five series was reacted for peroxidase activity
with the tetramethylbenzidine (TMB) method of Mesulam (1978)
and counterstained with neutral red.
Introduction
The striatum is an integral component of saccadic eyemovement circuits (see Hikosaka 2000). The inputs underlying particular motor, sensory, and cognitive activities of visuo/oculomotor neurons in the caudate are poorly understood. While corticostriate projections are
thought to provide saccade-related information to caudate neurons (Hikosaka et al. 1989), the role of thalamoJ.K. Harting (✉) · B.V. Updyke · D.P. Van Lieshout
Department of Anatomy, University of Wisconsin,
Madison, WI 53706, USA
e-mail: [email protected]
Fax: +1-608-2627306
Results
The left column in Figs. 1 and 2 shows the locations of
retrogradely labeled cells following an injection of
WGA-HRP into the visual-recipient sector of the caudate
nucleus (Updyke 1993). Within the thalamus, extensive
regions of the intralaminar complex contained dense
concentrations of labeled cells, especially the central anterior, rhomboidalis, central dorsal, and paraventricular
nuclei. Scattered cells also lay within the centromedian
nucleus as well as in the ventral region of the parafascicular nucleus and the nucleus limitans.
139
The lateral thalamus contained significant numbers of
labeled cells. In particular, there was a rostral band of labeled cells within the medial part of the ventroanterior
nucleus, which extended into the lateral ventromedial
nucleus; a few scattered cells were also present in the
Fig. 1 Legend see page 140
ventrolateral nucleus. Just as conspicuous were the numerous labeled cells in the lateral posterior complex. Using the terminology of Updyke (1983), the dorsal, medial, and ventral divisions of the lateral posterior shell and
the rostral division of the lateral zone contained labeled
140
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striatal projecting cells. At more caudal levels, retrograde labeling was also present within the lateral posterior shell, the rostral division of the lateral zone, and the
interjacent and medial zones. The suprageniculate nucleus also contained heavy labeling rostrally and more
sparse label caudally. Scattered labeled cells were also
present within the posterior nuclear group, the caudal division of the lateral zone of the lateral posterior nucleus
(LP), and the pulvinar nucleus. Data from other experiments (not illustrated) indicate that the characteristic pattern of afferent (and efferent) subcortical connections of
the visual-recipient zone is distinct from the adjacent somatosensory/motor region.
The right column in Figs. 1 and 2 shows the distribution of ascending anterogradely transported WGA-HRP
from the SC (and the locations of tectopetal cell bodies).
These projections were also more robust than previous
reports indicate (see Huerta and Harting 1984). Ascending SC input reached almost all of the thalamic cell
groups that project to the visual striatum. Thus, anterograde labeling was evident within the ventromedial and
ventrolateral nuclei, nucleus limitans, and the central
dorsal nucleus. Sparser label overlied the centromedian
nucleus, and there were dense patches of labeled processes overlying the central lateral nucleus. WGA-HRPpositive axons/terminals were also associated with the
intermediate division of the posterior nuclear group, suprageniculate nucleus, and the interjacent and medial
zones of the LP complex. Anterograde label lied over the
rostral division of the lateral zone of the LP complex and
the ventral division of the lateral posterior shell. Labeled
axons encroached upon the caudal division of the lateral
zone, along its border with the interjacent zone of the LP
Fig. 1 Illustrations showing the locations of anterogradely labeled
axons/terminals (black lines) and retrogradely labeled cells (black
circles) following injections of wheat-germ agglutinin/horseradish
peroxidase (WGA-HRP) into the visual-recipient caudate (left column) and superior colliculus (right column). AC Anterior commissure, AM anteromedial nucleus, AV anteroventral nucleus, Cd central dorsal nucleus, CD caudate nucleus, Cl central lateral nucleus,
Cm central medial nucleus, CM centromedian nucleus, d dorsal division of the medial geniculate nucleus, DHA dorsal hypothalamic
area, EN entopeduncular nucleus, Fr, Fx fornix, GP globus pallidus, LD laterodorsal nucleus, LGNd dorsal lateral geniculate nucleus, LGNv ventral lateral geniculate nucleus, Li nucleus limitans,
LPi interjacent zone of lateral posterior nucleus, LPl-c lateral zone
of lateral posterior nucleus, caudal division, LPl-r lateral zone of
lateral posterior nucleus, rostral division, LPm medial zone of lateral posterior, LPs-d lateral posterior shell, dorsal division, LPs-v
lateral posterior shell, ventral division, mc magnocellular division
of medial geniculate nucleus, MD mediodorsal nucleus, MTT
mammillothalamic tract, Ocn oculomotor nucleus, OT optic tract,
P pulvinar nucleus, PAG periaqueductal grey, Pf parafascicular nucleus, POi posterior nuclear group, intermediate division, POm
posterior nuclear group, medial division, PU putamen, PV paraventricular nucleus, R red nucleus, Sg suprageniculate nucleus,
SNc substantia nigra pars compacta, SNr substantia nigra pars reticulata, TRc thalamic reticular nucleus, v ventral divison of the medial geniculate nucleus, VA ventroanterior nucleus, VL ventrolateral nucleus, VM ventromedial nucleus, VPL ventroposterolateral
nucleus, VPM ventroposterior medial nucleus, VTA ventral tegmental area, ZI zona incerta
complex. Label present in the pulvinar and parvocellular
layers of the dorsal lateral geniculate nucleus can be attributed to the involvement of the pretectum in the injection site.
Discussion
The distribution of thalamostriate projections observed
in the current analysis is more extensive than reported in
previous studies of the caudate nucleus (see Mengual et
al. 1999 for a review). The intralaminar as well as several motor-related nuclei have been labeled in most of
these earlier studies (as well as in ours), so it is the additional widespread distribution of caudate-projecting cells
throughout the lateral (primarily visual) thalamus that
distinguishes the visual-recipient striatum. The fact that
the visual striatum was not specifically injected in most
earlier reports (see, however, Takada et al. 1985) explains the absence of thalamostriate cells in the visual
thalamus in such analyses. These data support the idea
that functionally distinct sectors of the striatum exhibit
different patterns of thalamostriate projections (Mengual
et al. 1999).
Superimposing the distributions of visual striate-related thalamostriate neurons (left column of Figs. 1 and 2)
and ascending tectothalamic axons/terminal (right column of Figs. 1 and 2) indicates that all of the former are
overlapped by the latter. While double-labeling studies
are needed to more accurately demonstrate this overlap,
the data certainly suggest that the SC is strategically positioned to influence all thalamic signals reaching the visual striatum. Some of these tectally innervated thalamic
nuclei, for example the ventromedial nucleus (VM), are
direct targets of the basal-ganglia outflow streams arising in the entopeduncular nucleus (EN) and the substantia nigra pars reticulata (SNr; Hendry et al. 1979). These
outflow signals reaching VM can be sent back to the striatum as part of a feedback circuit informing the striatum
about basal-ganglia signals reaching the cerebral cortex
(Mengual et al. 1999). Ascending tectal signals could
play a role in this proposed thalamostriate feedback loop.
Moreover, descending cortical as well as ascending brain
stem inputs that reach the SC (see Huerta and Harting
1984; Harting et al. 1992) could ultimately influence the
message sent from the VM to the visual-recipient striatum.
While basal-ganglia-outflow pathways directly innervate the VM, the cell groups of the LP-posterior nucleus
complex, which give rise to a far larger portion of the
thalamostriate projection to the visual-recipient striatum,
lack well-substantiated direct input from EN or SNr (see,
however, Takeda et al. 1984). Instead, these nuclei are
dominated by ascending tectal (Huerta and Harting
1984) and descending cortical inputs (Updyke 1981,
1983). These connectional differences indicate that information reaching the visual-recipient striatum from the
VM and LP complex differ even though ascending tectal
projections reach both regions. Moreover, these ascend-
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Fig. 2 Illustrations showing the locations of anterogradely labeled
axons/terminals (black lines) and retrogradely labeled cells (black
circles) following injections of WGA-HRP into the visual-recipient caudate (left column) and superior colliculus (right column).
Abbreviations as in Fig. 1
ing tectothalamic signals would be modulated by the nigrotectal projection. Thus, the striatonigro-nigrotectal projections would convey the output signal of the basal ganglia to the SC, where such information would modulate
ascending tecto-thalamic pathways and, thus, the information reaching the visual-recipient striatum via direct
thalamostriate and indirect thalamo-corticostriate paths.
Most importantly, the SC signals conveyed to the visualrecipient striatum reflect the ongoing activity in the SC,
which involves both the integration of visual, oculomotor, auditory, and somatosensory signals, and their modulation by striato-nigro-tectal pathways.
It is noteworthy that the striatonigral projection labeled following WGA-HRP injections into the visualrecipient striatum (Fig. 2, left column) only partially
overlaps the locations of retrogradely labeled nigrotectal
neurons seen in the experiments involving injections of
WGA-HRP into the SC. Functionally distinct striatal
sectors project to distinct non-overlapping regions of the
SNr (see Maurin et al. 1999), and different parts of the
SNr innervate (and modulate) distinct layers and sublayers of the SC (Harting et al. 1988). Since cells in the latter area target different thalamic cell groups innervating
both cortical areas and the visual-recipient striatum, it
follows that the different thalamofugal projections may
be selectively influenced by outflow channels of different functional sectors of the caudate (and putamen; see
Updyke 1993). This would facilitate associative “cross
talk” within the striatum and the different parallel functional circuits (Alexander et al. 1986).
In summary, these findings suggest a broader influence of the superior colliculus on thalamostriate circuitry
and on visual/oculomotor-striatal function(s). Basal-ganglia outflow reaching the SC via striatonigro-nigrotectal
circuitry not only influences the SC projections that descend to eye-movement centers in the brain stem (see
Huerta and Harting 1984), but, just as important, regulate different ascending tectothalamic pathways. The evi-
142
dence presented here for relatively robust and direct
tecto-thalamostriate projections suggests to us that the
constraints placed upon tectal processing by striatonigral
control have important consequences for central perceptuomotor processing at the sriatal and cortical levels.
Acknowledgements Supported by Grant NS-37445 to JKH and
EY05724 to BVU. We thank Cheryl Vega for technical support.
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