Download Do superior colliculus projection zones in the inferior pulvinar

© European Neuroscience Association
European Journal of Neuroscience, Vol. 11, pp. 469–480, 1999
Do superior colliculus projection zones in the inferior
pulvinar project to MT in primates?
Iwona Stepniewska, Hui-Xin Qi and Jon H. Kaas
Department of Psychology, Wilson Hall, Vanderbilt University, Nashville, TN 37240 USA
Keywords: ascending projection, extrastriate cortex, lateral geniculate nucleus, monkey, posterior thalamus
Abstract
In order to determine the relationship of superior colliculus inputs to thalamic neurons projecting to the middle temporal visual area
(MT), injections of wheat germ agglutinin conjugated with horseradish peroxidase were placed in the superior colliculus of three
owl monkeys, with injections of Fast Blue in the MT. The locations of labelled terminals and neurons in the posterior thalamus
were related to four architectonically distinct nuclei of the inferior pulvinar (Stepniewska & Kaas, Vis. Neurosci. 14, pp.1043–
1060, 1997). Fast Blue injections in the MT labelled neurons largely in the medial nucleus of the inferior pulvinar. A few labelled
neurons were found in the adjoining central medial nucleus of the inferior pulvinar, as well as in the lateral pulvinar and the dorsal
lateral geniculate nucleus. Superior colliculus inputs were most dense in the posterior and medial nuclei of the inferior pulvinar.
There were sparser inputs to the central lateral nucleus of the inferior pulvinar, locations in the lateral and medial pulvinar, and the
dorsal lateral geniculate nucleus. The results indicate that the medial nucleus of the inferior pulvinar, the major projection zone to
the MT, does not receive a significant input from the superior colliculus.
Introduction
Traditionally, the pulvinar complex of the dorsal thalamus has been
divided into the inferior, lateral, medial and, sometimes, anterior
divisions (see Kaas & Huerta, 1988). Although all of these large
divisions probably have functionally significant subdivisions, the most
compelling evidence has been for the inferior pulvinar, where several
nuclei or subnuclei have been distinguished on the basis of architectonic distinctions and differences in connections. Nearly 30 years
ago, Mathers (1971) reported that the superior colliculus projections
were unevenly distributed in the inferior pulvinar with a concentration
of inputs in a medioposterior region distinguished as a ‘posterior’
nucleus. Soon thereafter, Spatz & Tigges (1973) described projections
from the middle temporal visual area (MT), as most dense in a medial
portion of the inferior pulvinar, just lateral to the ‘posterior’ nucleus
of Mathers (1971). Next, Lin et al. (1974) found that injections of
the newly available retrograde tracer, horseradish peroxidase, into the
MT labelled the same medial zone of the inferior pulvinar. In
subsequent studies, Lin & Kaas (1979, 1980) concluded that the
boundaries of these nuclei in the inferior pulvinar could be distinguished in myelin preparations by encapsulating fibre bands. A
posterior nucleus of the inferior pulvinar (which they labelled IPp),
corresponded to the posterior nucleus of Mathers (1971), and a central
nucleus (their IPc), received inputs from the superior colliculus and
projected to more rostral and more caudal divisions of visual cortex,
respectively. A medial nucleus (their IPm) was described as devoid
of superior colliculus inputs, while projecting densely to the MT.
Thus, no part of the inferior pulvinar complex provided a significant
relay of visual information from the superior colliculus to the MT.
Recently, there have been reasons to question the basic proposal
Correspondence: Dr Jon H. Kaas, as above.
E-mail: [email protected]
Received 20 May 1998, revised 7 September 1998, accepted 10 September 1998
that three nuclei subdivide the inferior pulvinar, with none of the
three providing a significant relay of superior colliculus information
to the MT. First, re-examinations of the architecture of the inferior
pulvinar, using a range of current histochemical techniques, have
revealed further subdivisions. In our recent re-interpretation of the
organization of the inferior pulvinar (the original IPc) has been
divided into central medial and central lateral nuclei or subnuclei
(which we refer to as PICM and PICL) while the medial and posterior
nuclei of the inferior pulvinar (PIm and PIp) are retained, resulting
in four quite distinguishable structures (Stepniewska & Kaas, 1997).
Gutierrez et al. (1995) had previously used similar histochemical
procedures to divide the PIc into three subdivisions, a ‘PIc’ corresponding to our PICM, a ‘PIL’ largely corresponding to our PICL, and
a narrow, lateral shell. Both Gutierrez et al. (1995) and an earlier
study of Cusick et al. (1993) provided valuable information on
the histochemical characteristics of the PIm and PIp. These new
interpretations of how the inferior pulvinar is subdivided raise new
questions about how these redefined subdivisions relate to inputs
from the superior colliculus and to cortical targets, such as the MT.
While the evidence across primate species is rather compelling for
the conclusion that one of these subdivisions, the PIm, projects
preferentially to the MT (see Cusick et al., 1993 for review), the PIm
is in a location that could correspond to the site of dense inputs from
the superior colliculus (see Gutierrez et al., 1995; for review). Cusick
et al. (1993) noted that histochemical features of the PIm, such as
dense staining for cytochrome oxidase (CO) and parvalbumin, and
light staining for calbindin, are characteristics of the relay nuclei
of the thalamus, such as the ventroposterior nucleus. Thus, the
histochemical features suggest that the PIm could function as a relay
nucleus by receiving inputs from the superior colliculus and projecting
to the MT.
Another reason to consider the possibility that the superior colliculus
relays to the MT through the inferior pulvinar is the evidence that
470 I. Stepniewska et al.
the MT can be quite responsive to visual stimuli after lesions of
striate cortex. Rodman et al. (1989) found that many neurons in the
MT of macaque monkeys were responsive to visual stimuli after
removal of striate cortex, and that some neurons even retained at
least some of their normal response properties, such as selectivity for
direction of movement. Furthermore, lesions of the superior colliculus,
in conjunction with striate cortex lesions, abolished responsiveness
to visual stimuli (Rodman et al., 1990). The most reasonable interpretation of these findings is that the superior colliculus relays visual
information to the MT via projections to the pulvinar, and that this
relay adequately activates the MT in the absence of primary visual
area (striate cortex, V1). As the target of the most dense inputs from
the superior colliculus, the inferior pulvinar would be the likely
source of the relay.
In the present study, we sought to resolve some of the questions
concerning possible relay of superior colliculus information to the
MT by studying pulvinar connections with the superior colliculus and
with the MT in the same animals. In addition, we used histochemical
procedures to define the currently proposed subdivisions of the
inferior pulvinar. Finally, we studied owl monkeys, the primate from
which the evidence that the inferior pulvinar does not provide a
significant relay of visual input from the superior colliculus to the
MT was originally gathered, so that early and present results could
be directly compared.
Materials and methods
Connections of the pulvinar were studied in three adult owl monkeys
(Aotus trivirgatus) by placing injections of tracers into the superior
colliculus and the MT under aseptic conditions. Results were related
to recently described architectonic subdivisions of the inferior pulvinar
(Stepniewska & Kaas, 1997).
Surgery and injections
Monkeys were anaesthetized for surgery with intramuscular injection
of a mixture of ketamine hydrochloride (30 mg/kg) and xylazine
hydrochloride (1–2 mg/kg), supplemented as needed to maintain a
surgical level of anaesthesia or replaced with 2% isoflurane as an
inhalation anaesthetic. The head was fixed in a stereotaxic apparatus,
and a portion of posterior parietal and visual cortex was exposed
during aseptic surgery. In each case, a low-impedance microelectrode
was lowered through posterior parietal cortex to the superior colliculus,
using stereotaxic measurements from the brain sections of four owl
monkeys processed for other studies. After recordings of visually
evoked multineuron activity were used to establish the location of
the superior colliculus, several additional electrode penetrations were
made to determine its approximate rostral, caudal and lateral boundaries. Next, a bevelled Hamilton microsyringe, with a microelectrode
glued to the needle, was filled with a solution of 2% wheat germ
agglutinin conjugated with horseradish peroxidase (WGA-HRP) in
saline. The microsyringe was then lowered to the previously determined level of the superior colliculus and adjusted until adequate
visually evoked responses were recorded from the attached microelectrode. Then, µ 0.1 µL of tracer solution was injected, and the
microsyringe was removed after 15–20 min. Next, the fluorescent
tracer, Fast Blue (FB) was pressure-injected into the MT by using a
glass micropipette attached to a Hamilton syringe. Approximately
0.2–0.4 µL of 2% FB in saline was injected in the location of the
MT, which was estimated by its position relative to the caudal tip of
the superior temporal sulcus (Allman & Kaas, 1971). The micropipette
was removed after 15–20 min. The exposed cortex was covered with
gelatin film, the skull opening sealed with an artificial bone flap made
of dental cement, and the skin sutured. Animals were carefully
monitored during recovery from anaesthesia, and they received
antibiotics and analgesics.
After 4–5 days, the animals were deeply anaesthetized and perfused
through the heart with saline followed by 2% paraformaldehyde in
saline as a fixative, followed by 10% sucrose in fixative. The brain
was removed and cortex was separated from the brainstem, and
manually flattened between glass slides. The cortex and brain stem
were stored in 30% sucrose in the refrigerator overnight.
Histology and anatomical analysis
Twelve to 24 h after perfusion, the cortex and brainstem (including the
thalamus) were cut into 40–50-µm sections on a freezing microtome. A
block of flattened cortex containing the MT and other visual areas
was cut parallel to the surface, and divided into three series of
sections. One series was mounted on glass slides and coverslipped
without further processing so that neurons labelled with FB could be
located. Another series was processed for myelin according to the
procedure of Gallyas (1979), and the third series was processed for
CO following the procedures of Wong-Riley (1979). Both the myelin
and CO procedures allowed us to identify the MT as a darker oval
in the processed sections (see Krubitzer & Kaas, 1990) and to locate
the injection sites relative to the MT boundaries.
The brainstem through the midbrain and thalamus was cut in the
coronal plane and divided into five separate series of every fifth
section. One series was mounted and coverslipped without further
processing so that neurons labelled by retrogradely transported FB
could be visualized. Another series of sections was histochemically
processed to reveal WGA-HRP according to the procedures of Gibson
et al. (1984). The remaining sections were processed to reveal
subdivisions of the inferior pulvinar (see Stepniewska & Kaas,
1997). One series was treated histochemically for acetylcholinesterase
(AChE) using the protocol of Geneser-Jensen & Blackstad (1971),
and another for CO (Wong-Riley, 1979). The last series was processed
immunocytochemically for the calcium-binding protein, CalbindinD28K (Cb) (Celio, 1990). Brainstem sections were drawn through a
drawing tube with a Wild macroscope, and regions of WGA-HRP
label were located under darkfield illumination. The distributions of
neurons labelled with FB were charted with a fluorescent microscope.
Sections processed for AChE, CO, or Cb were drawn at the same
magnification, and boundaries of pulvinar subdivisions were outlined.
These boundaries were then superimposed on the drawings of labelled
neurons and terminals using adjacent brain sections. A surface view
of the superior colliculus was reconstructed from serial sections, and
the region labelled by each injection was determined relative to visual
hemifield coordinates superimposed from standardized retinotopic
maps of the superior colliculus of owl monkeys (Lane et al., 1973).
The injection sites of FB were localized within the architectonic
boundaries of the MT that were determined by aligning drawings of
the injection sites and CO-and myelin-based boundaries.
Results
Injections of WGA-HRP were placed in the superior colliculus of
the same three owl monkeys in which FB had been placed in the
MT. The resulting patterns of labelled neurons from the FB injection
and terminals from the WGA-HRP injections were related to the
architecture of the pulvinar complex and the adjoining dorsal lateral
geniculate nucleus (LGNd). The results indicate that there is little
overlap in the pulvinar between superior colliculus inputs and neurons
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
Superior colliculus projections 471
FIG. 1. Darkfield photomicrographs of the coronal sections through the pulvinar in Case 97-53. Top panel: adjacent sections through the inferior pulvinar (A)
showing the distribution of anterogradely labelled superior colliculus terminals and (B) stained for CO. Note that CO-dark PIm is free of label, and laterally
adjacent CO-lighter PICM is full of labelled terminals. Bottom panel: sections from the different levels of the inferior pulvinar with anterogradely labelled
terminals distributed in (C) the PIp, (D) the PIp and PICM with a visible fusion zone below the PIm and (E) the PICM and PL. Note the label of fibres coursing
through the PIm in C and D. In E, the label in the PL is patchy and much sparser than in the PICM. The thin black line marks the region of labelled fibres.
Scale bar 5 500 µm.
projecting to the MT. More specifically, the PIm constitutes the major
projection nucleus to the MT, but the PIm receives little or no input
from the superior colliculus. Results supporting these and other
conclusions are presented in three parts. First, we briefly present the
architectonic evidence that was used to subdivide the pulvinar.
Secondly, we describe the superior colliculus projections to the
posterior thalamus. Next, we indicate where neurons projecting from
the pulvinar to the MT are located. Finally, superior colliculus inputs
to the LGNd and LGNd projections to the MT are described.
Architectonic subdivisions of the pulvinar
Our material revealed four distinct regions of the inferior pulvinar
complex. We have recently described the architecture of these regions
in owl monkeys, squirrel monkeys and macaques (Stepniewska &
Kaas, 1997), and the present results closely conform to this previous
account. The most significant of these subdivisions is PIm, since it
has been considered to be the main source of projections to the MT
(e.g. Lin & Kaas, 1980). PIm was dark and patchy in CO and AChE,
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
472 I. Stepniewska et al.
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
Superior colliculus projections 473
and light in Cb preparations. Examples of the appearance of PIm in
CO sections are shown relative to distributions of terminals labelled
by WGA-HRP in Fig. 1 (A and B). More medially, the posterior
nucleus, PIp, was dark for Cb, and moderate for CO and AChE.
More laterally, the medial central nucleus, PICM, was dark for Cb
and light for AChE and CO. Most laterally, the lateral central nucleus,
PICL, was dark for AChE and moderate for CO and Cb. Overall, the
differences in appearance between the four nuclei were obvious, and
there was no chance of misidentification. Most importantly, the newly
proposed subdivision, PICM, was distinct from PIm.
Projections of the superior colliculus
Projections of the superior colliculus to the pulvinar complex were
studied after large injections of WGA-HRP into the superior colliculus
of three owl monkeys. The full extent of the injections varied,
however, with the largest injection occurring in Case 97-53, where
the superficial layers were densely labelled throughout all but the
most rostral fringe of the superior colliculus (Fig. 2A). In addition,
the deep layers of the superior colliculus and part of the inferior
colliculus were labelled in this case. A somewhat smaller zone of
dense label was found in Case 96-89 (Fig. 3A). While the densely
labelled zone included all but the most rostral part of the medial
superior colliculus, less of the rostrolateral superior colliculus was
included. Yet, projections would involve large parts of the representations of both the upper and lower visual quadrants in this case. Here,
only the superficial layers of the superior colliculus were densely
labelled. In the third case, 96-82 (Fig. 4A), the dense label from the
injection covered much of the lateral part of the superior colliculus
representing the upper visual quadrant, and only lighter, diffuse label
was found in the medial part of the superior colliculus. Projections
in this case were probably restricted to those from the representation
of the upper visual quadrant.
The overall pattern of projections from the superior colliculus to
the pulvinar was demonstrated most effectively in Case 97-53, which
had the largest injection site (Fig. 2A). In this case, transported label
reflecting terminations (Fig. 2C) was exceedingly dense throughout
most of the PICM and PIp (Fig. 1A and C–E). Regions of moderate
to light concentrations of label occurred in the PICL and in the lateral
pulvinar (PL) (Fig. 1E). Label in the medial pulvinar (PM) was sparse
and scattered. Thus, most of the label was in the PICM and PIp of
the inferior pulvinar. The zones of label in the two nuclei appeared
to fuse ventrally in the caudal thalamus (see section 92, Fig. 1D),
suggesting either the course of entering fibres of passage, or that the
PIm does not extend to the ventral margin of the pulvinar in this
location. The zones of label in the PICM and PIp also extended
dorsally past the brachium of the superior colliculus, the traditional
dorsal boundary of the inferior pulvinar, in agreement with the
compelling architectonic evidence that both of these nuclei extend
dorsally past the brachium (see Stepniewska & Kaas, 1997). Most of
the PIm and even the PICL were free of label. The sparse label that
was observed in parts of the PIm could easily reflect preterminal
fibres coursing to the PICM.
The transported label in the pulvinar was less extensively distributed
in Case 96-89 (Fig. 3), possibly because the dense injection core did
not involve the rostral superior colliculus representing the central 5°
of vision. The injection core was also superficial, with only limited
involvement of the deeper layers. Again, the label was most dense
in the PICM and PIp, but the label was concentrated ventrally, and it
did not extend dorsally across the brachium of the superior colliculus.
This observation is consistent with the premise that central vision is
represented dorsally in these two nuclei. Some label was apparent in
the PICM and in the caudal part of the PL; the PIm was devoid of
label, as was the entire medial pulvinar.
In Case 96-82, the injection core was confined to the lateral half
of the colliculus, and the dense label was in the superficial layers
(Fig. 4A). The transported label in the pulvinar complex was largely
confined to the PICM and PIp, with nearly all of the label in the
portions of these nuclei under the brachium of the superior colliculus
(Fig. 4C). In both nuclei, the label was mostly caudal, and more
medial caudally and more lateral rostrally. The results suggest that
the lower quadrant of the visual hemifield is represented across the
more caudal aspects of the PICM and PIp. A region of quite sparse
label was found in the medial part of the PICL, possibly reflecting
label in fibres terminating in the PICM. No label was noted in other
parts of the PICL, PL or PM.
Pulvinar projections to the MT
In all three monkeys, the injections of FB were located within the
MT as defined architectonically in sections cut parallel to the brain
surface. These sections allowed the MT to be outlined as an oval of
cortex that was more densely stained for myelin and CO.
In Case 97-53 (Fig. 2) the FB injection was placed centrally in the
MT in a location representing paracentral vision slightly into the
lower quadrant (Allman & Kaas, 1971). Most of the retrogradely
labelled neurons in the pulvinar complex were in the PIm, with
labelled neurons in both portions over and under the brachium of the
superior colliculus. A few labelled neurons were in the PICL and
possibly upper PICM, and several foci of labelled neurons were in the
PL. No labelled neurons were found in the PM.
Results from Case 96-89 (Fig. 3), with an injection in the lateral
MT, devoted to paracentral vision of the upper quadrant, were similar,
in that most of the labelled neurons were in the PIm, a few were in
the PICM and PICL, and several foci of labelled neurons were in the
PL. Unexpectedly, some labelled neurons were in the PM, and a few
were in the PIp. The labelled neurons in the PIm were largely below
the brachium of the superior colliculus and they were more caudal
than rostral in the nucleus. Labelled neurons were also most densely
distributed in the PIm of the third case, 96-82 (Fig. 4), where the
injection was placed in the rostral MT, which is devoted to peripheral
vision. However, in this case neurons labelled with FB were located
mainly in the upper portion of the PIm, above the brachium of
superior colliculus. Other labelled neurons were in the PICL, and a
few were in the PICM, PL and PM.
The LGN: superior colliculus inputs and projections to the MT
In two of three cases (97-53 and 96-89) superior colliculus injections
produced label in the LGNd, as well as the pregeniculate (PG) or
FIG. 2. The pattern of afferent and efferent pulvinar projections, originating from the superior colliculus and sent to the MT in Case 97-53. (A) The WGA-HRP
injection site in the superior colliculus is shown in coronal sections from posterior (26) to anterior (68). The effective injection site of dense label is dark while
the diffusion zone is hatched. (B) The FB injection site in the MT reconstructed from the sections of flattened cortex. (C) The distribution of anterogradely
labelled terminals after the superior colliculus injection (small dots) and retrogradely labelled neurons after the MT injection (large dots), shown on coronal
thalamic sections from posterior (80) to anterior (122). The boundaries of pulvinar subdivisions are marked with thin lines. Central (PIc), central lateral (PICL),
central medial (PICM), medial (PIm) and posterior (PIp) divisions of the inferior pulvinar are indicated.
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
474 I. Stepniewska et al.
FIG. 3. The pattern of pulvinar connections originating in the superior colliculus and sent to the MT in Case 96-89. Other conventions as in Fig. 2.
Superior colliculus projections 475
FIG. 4. The pattern of pulvinar connections originating in the superior colliculus and sent to the MT in Case 96-82. Other conventions as in Fig. 2.
476 I. Stepniewska et al.
ventral lateral geniculate nucleus (Figs 2, 3, 5 and 6). Because of the
large injection site in Case 97-53, the label was much more extensive
than in Case 96-89. However, in both cases the terminals of axons
coming from the superior colliculus were unevenly distributed,
aggregating in patches in the intercalated or koniocellular (K) LGN
layers (Hendry & Casagrande, 1996). The main focus of label was
always in the K1 (or S) layer (see Kaas et al., 1978) that lies next to
the optic tract. Smaller patches of label were found in layers K2,
between magnocellular (M) layers, and K3, between the M and
parvocellular (P) layers. In Case 97-53, the label was most extensive
at the most caudal LGN level, extending through its central level,
and the anterior LGNd was almost free of label (Fig. 5).
Injections in the MT in Case 97-53 labelled a few neurons in the
K layers or on the borders of M layers of the LGN (Fig. 5). The
terminals labelled in K layers after superior colliculus injections
partly overlapped with retrogradely labelled neurons, suggesting that
these connections form a pathway through which visual information
from the retina reaches area the MT. These neurons, however, were
not numerous, and some of them may not receive superior colliculus
inputs. In Case 96-89 (Fig. 6) the anterogradely labelled axonal
terminals were more restricted than in Case 97-53 and were found
only in the most caudal portions of the K1 and K2 LGN layers. At
the same level, few neurons labelled after the MT injections were
found at the border of the magnocellular layer receiving input from
the contralateral eye (Mc) and K2 layers (Fig. 6, section 147), and
they did not overlap with labelled superior colliculus terminals. We
did not find neurons labelled after the MT injections in Case 96-82.
Injections in the superior colliculus also labelled the PG. With
WGA-HRP, both anterogradely labelled terminals and retrogradely
labelled neurons were found, showing that connections between the
superior colliculus and the pregeniculate are reciprocal. The label
was very extensive in Case 97-53 (Fig. 5), covering almost the whole
extent of the PG. In Case 96-89 only scattered anterogradely labelled
terminals were found (Fig. 6).
Discussion
The present results demonstrate that the superior colliculus projects
most densely to the PIp and PICM nuclei of the inferior pulvinar
complex, and that the PIm nucleus, situated between them, provides
the main pulvinar projection to the MT. Thus, the PIm does not relay
superior colliculus information to the MT. The superior colliculus
also projects to other parts of the pulvinar complex, as well as the
LGNd. Some of these pulvinar regions and a few cells of the LGNd
project to the MT, providing sparse, but direct, pathways from the
superior colliculus to the MT.
Subdivisions of the pulvinar
Modern histochemical and immunocytochemical procedures clearly
reveal four distinct regions in the territory of the traditional inferior
pulvinar. Two of these subdivisions, the posterior (PIp) and medial
(PIm) nuclei of the inferior pulvinar, correspond to those previously
described by Lin & Kaas (1979, 1980). However, their third central
division (IPc) contains obvious medial and lateral subdivisions, which
we have termed PICM and PICL, to indicate that they were derived
from the original PIc (Stepniewska & Kaas, 1997). These subdivisions
are apparent in both New and Old World monkeys, and they were
first recognized by others (Gutierrez et al., 1995). Somewhat different
terminologies have been applied for the region of the original ‘PIc’
in a manner that has been inconsistent across species (see Stepniewska
& Kaas, 1997, for review). The present terminology avoids the
confusion of using the earlier term of ‘PIc’ in new and inconsistent
ways. Whether the subdivisions of the inferior pulvinar should be
considered as separate nuclei or subnuclei (layers) is another issue
(see Gutierrez et al., 1995), but we refer to the subdivisions as
nuclei simply for convenience. The PL and PM undoubtedly contain
subdivisions as well, but none have been clearly demarcated, and
quite possibly there are further subdivisions within the inferior
pulvinar. The important point here is that four subdivisions of the
inferior pulvinar are now obvious, and they can be related to superior
colliculus inputs and to the locations of neurons projecting to the MT
(for a schematic description of different proposed subdivisions of the
inferior pulvinar in owl, squirrel and macaque monkeys, see fig. 16
of Stepniewska & Kaas, 1997).
Projections of the PIm and other parts of the pulvinar to the
MT
In each of the three cases with MT injections, most of the labelled
neurons were in PIm. In these cases, the PIm was identified as
calbindin-poor and AChE- and CO-rich. Thus, there was no doubt
about which nucleus provided the major projection to the MT. The
PIm, of course, has not been identified by such criteria in previous
studies of thalamic projections to the MT, but it has been clear that
the projections have been either from the PIm or a very similar region
of the thalamus. In the original study of pulvinar projections to the
MT in primates, the medial location of the projection zone in the
inferior pulvinar was stressed, and the suggestion was made that this
medial group of cells form a separate nucleus that projects to the MT
(Lin et al., 1974). Later, these projecting neurons were related to a
medial subdivision of the inferior pulvinar, the PIm, that was apparent
in brain sections stained for myelin, since encapsulating fibre bands
separated the PIm from the smaller PIp on its posterior-medial border
and a larger PIc on its lateral border (Lin & Kaas, 1979). By
comparing brain sections processed for myelin with those processed
for Cb, AChE or CO in the same owl monkeys, we showed that the
encapsulated PIm of owl monkeys is Cb-poor, AChE-rich and
CO-rich (Stepniewska & Kaas, 1997). The PIm has also been
distinguished by Cb, AChE and CO procedures in squirrel monkeys
and macaque monkeys (Cusick et al., 1993; Gutierrez et al., 1995;
Stepniewska & Kaas, 1997). In squirrel monkeys, the PIm is the
region of the pulvinar that is the most densely interconnected with
the MT (Spatz & Tigges, 1973; Cusick et al., 1993), and the PIm
region has been shown to have dense MT connections in macaque
monkeys (Standage & Benevento, 1983; Ungerleider et al., 1984;
however, see Maunsell & Van Essen, 1983), marmosets (Dick et al.,
1991) and galagos (Wall et al., 1982). Thus, it seems clear that the
major connections of the MT with the pulvinar are with the PIm.
Our MT injections also labelled some neurons in the PICM, PICL
and PIp. In previous studies horseradish peroxidase injections in the
MT resulted in few or no labelled neurons in the PIc and PIp (Lin
& Kaas, 1980), but FB may be more sensitive as a retrogradely
transported marker. Another possibility is that terminals just outside
the MT took up some of the FB, but there was no indication of that
possibility from our examinations of the injection sites. However, the
PIc and PIp do project to the cortex surrounding the MT (Lin &
Kaas, 1979; Steele et al., 1991; Cusick et al., 1993). We conclude
that the PIp and PIc probably project to the MT, but this projection
is sparse and possibly variable across species and individuals.
Injections of FB also labelled foci of neurons in the PL. In previous
studies in squirrel monkeys, injections involving the MT, as well as
cortex caudal to the MT, labelled neurons in the PL (Cusick et al.,
1993), and the MT clearly projects to the PL in macaques (Ungerleider
et al., 1984), squirrel monkeys (Spatz & Tigges, 1973) and galagos
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
Superior colliculus projections 477
FIG. 5. The pattern of LGN connections originating in the superior colliculus and sent to the MT in Case 97-53, shown in a series of coronal sections arranged
from posterior (128) to anterior (164). Anterogradely labelled terminals after superior colliculus injections are marked with small dots, and retrogradely labelled
neurons after the MT injections are marked with large dots. The LGNd layers are marked with thin lines. The koniocellular, magnocellular and parvocellular
layers are designated K, M, and P, respectively. The ‘c’ layers are those receiving input from the contralateral eye, the ‘i’ layers are those receiving input from
the ipsilateral eye. In the PG, the WGA-HRP anterogradely labelled terminals overlapped with the WGA-HRP retrogradely labelled neurons. For clarity the
retrogradely labelled neurons are not marked.
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
478 I. Stepniewska et al.
FIG. 6. The pattern of LGN connections originating in the superior colliculus in Case 96-89 shown on coronal sections arranged from posterior (142) to anterior
(152). Other conventions as in Fig. 5.
(Wall et al., 1982). Since corticothalamic connections are expected
to be reciprocal, it is likely that the PL projects to the MT in all
these primates. The projection neurons in owl monkeys were scattered,
and not numerous. The separate foci may relate to proposed subdivisions of PL (Stepniewska & Kaas, 1997; Beck & Kaas, 1998;
see also Wong-Riley, 1977), but these results do not provide clear
evidence for such subdivisions.
Superior colliculus inputs to the pulvinar
Our results provide compelling evidence that the major projections
from the superior colliculus to the pulvinar complex are to the PIp,
PICM and PICL, much as Lin & Kaas (1979) had described earlier.
By injecting tracers into the superior colliculus and the MT of the
same monkeys, we were able to demonstrate that the superior
colliculus projections were very sparse in the zone where dense MT
projections originate in the inferior pulvinar, and our architectonic
analysis in these monkeys allowed the four nuclei of the inferior
pulvinar to be reliably identified. We conclude that PIm does not
provide a relay of superior colliculus visual information to the MT,
at least in owl monkeys.
The importance of resolving this issue lies in the considerable
uncertainty over the possibility of a major relay of superior colliculus
inputs from the inferior pulvinar to the MT. The superior colliculus
inputs have been described as densely distributed to both lateral and
medial sectors of the inferior pulvinar, allowing for the possibility
that there is considerable overlap, rather than complete segregation,
in the inputs and the projections to the MT. Indeed, Cusick et al.
(1993) have noted that the dense CO and parvalbumin staining and
calbindin-poor nature of the PIm are highly suggestive of a primary
sensory relay nucleus, such as the ventroposterior nucleus or the
lateral geniculate nucleus (LGN). They also noted that the tectorecipient zones in the inferior pulvinar of macaque monkeys (Benevento
& Fallon, 1975; Harting et al., 1980; Benevento & Standage, 1983)
and squirrel monkeys (Mathers, 1971), based on location, seem likely
to include the PIm. Furthermore, Raczkoski & Diamond (1980) have
previously concluded that the tectorecipient zone of galagos projects
to the temporal lobe, ‘probably’ the MT. While evidence for such a
relay in these other primates needs to be directly examined, since
primate taxa could differ, there is no compelling evidence for this
relay in any primate. Rather, the approximation of the two projection
zones, together with little evidence for how the superior colliculus
inputs relate to the chemoarchitecture of the inferior pulvinar, allowed
several possible interpretations of connection patterns.
The present results suggest that we reconsider the sources of
activation of the MT in the absence of V1. Rodman et al. (1989)
reported that considerable responsiveness to visual stimuli remained
for MT neurons after striate cortex removal. Furthermore, this
responsiveness disappeared after superior colliculus lesions in such
monkeys (Rodman et al., 1990). These results suggested the need for
a direct tectopulvinar pathway that is capable of activating MT
© 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 469–480
Superior colliculus projections 479
neurons, and preserving considerable visual functions in the absence
of V1. Such a pathway has also been suggested for the preservation
of visual abilities in brain-damaged patients that demonstrate aspects
of preserved vision known as blindsight (see e.g. Cowey & Stoerig,
1991). The results of Rodman et al. (1989) seem to differ from those
of Maunsell et al. (1990) who reported that blocking LGN activity
in macaques ‘essentially eliminated’ the evoked activity of MT
neurons. Kaas & Krubitzer (1992) found that striate cortex lesions
deactivated MT neurons in owl monkeys. The reasons for these
seemingly different results remain unclear, but the present results
suggest that any role for the superior colliculus in MT activity does
not involve a direct tecto-pulvinar–MT relay. While some overlap of
sparse inputs from the superior colliculus with neurons in the pulvinar
may occur, especially in the PL, these connections would seem to be
too few projecting to the MT to substitute for the striate cortex inputs.
Instead, the substantial projections from the PIc and PIp to cortical
areas that are interconnected with the MT are more likely to play
this role.
Our results suggest that the main thalamic inputs from the superficial
layers of the superior colliculus are to the inferior pulvinar. Labelled
terminals were found outside the inferior pulvinar in the PL in only
one of our two cases with superficial injections. However, more foci
of labelled terminals were apparent in the PL of our case with the
largest injection, that involved both superficial and deep layers.
Additional foci were in the PM. In both squirrel monkeys (Harting
et al., 1978; Huerta & Harting, 1983) and macaques (Harting et al.,
1980), the superior colliculus clearly projects to the PL, although
these projections are not always obvious (Partlow et al., 1977). Some
label was apparent in the PM after injections in the superior colliculus
in both squirrel and macaque monkeys (Harting et al., 1978, 1980).
The PM is usually considered a target of only the deeper layers of
the superior colliculus (see Kaas & Huerta, 1988).
Since the MT injections labelled neurons in the PL that were
occasionally overlapped by superior colliculus inputs, a pathway does
exist for the direct activation of MT neurons via a tecto-pulvinarpathway connection. However, this pathway would probably have
only weak effects on the MT because of the sparseness of the superior
colliculus inputs and the limited numbers of PL neurons projecting
to the MT.
A tecto-geniculo-cortical path to the MT
Our superior colliculus injections also revealed projections to the
LGNd. These inputs are known to originate from the superficial grey
layer and terminate most densely on the interlaminar zones and the
ventrally located superficial ‘S’ layers (Harting et al., 1978, 1980),
and are likely to activate the koniocellular or small cell relay in the
LGNd that projects to superficial layers of striate cortex (Casagrande
& Kaas, 1994; Casagrande, 1994). Our MT injections labelled a few
large neurons in the LGNd that were distributed near, or in, the
interlaminar zones, and these neurons are possibly activated by
superior colliculus inputs. Although the vast majority of LGN neurons
in primates project to V1, a few have been shown to project to the
secondary visual area (prestriate cortex, V2) (Bullier & Kennedy,
1983), dorsolateral visual cortex (Lysakowski et al., 1988; Cowey &
Stoerig, 1989), the dorsomedial visual area (Beck & Kaas, 1998), the
MT (Fries, 1981), and even inferior temporal cortex (HernandezGonzalez et al., 1994; however, see Sorenson & Rodman, 1996).
Projections from the LGNd to the MT might be expected from early
evidence that the MT projects to the LGNd (Lin & Kaas, 1977;
Graham et al., 1979; however, see Ungerleider et al., 1984) and the
evidence that connections between visual structures are usually
reciprocal (see Felleman & Van Essen, 1991). Such extrastriate
projections of the LGNd have been postulated as important in
mediating aspects of vision in extrastriate cortex after lesions of V1
(Cowey & Stoerig, 1989), but the ones to the MT constitute a very
sparse and probably ineffective source of direct activation for MT
neurons after lesions of V1 (Rodman et al., 1989).
Acknowledgements
We thank Judy Ives and Laura Trice for technical assistance. Helpful comments
in the manuscript were provided by Pam Beck, Troy Hackett, Fabrizio Strata
and Hilary Taub. The research was supported by NEI Grant EY 02686.
Abbreviations
AChE, acetylcholinesterase; c, (suffix) contralateral; Cb, Calbindin-D28K;
CO, cytochrome oxidase; FB, Fast Blue; i, (suffix) ipsilateral; K, koniocellular
layer of the LGN; LGN, lateral geniculate nucleus; LGNd, dorsal LGN; M,
magnocellular (layer); MT, middle temporal visual area; P, parvocellular
(layer); PIm, medial nucleus of the inferior pulvinar; PIc, original nomenclature, largely corresponds to PICM here; PIL, original nomenclature, largely
corresponds to PICL here; PICM, central medial nucleus of the inferior pulvinar;
PICL, central lateral nucleus of the inferior pulvinar; PIp, posterior nucleus of
the inferior pulvinar; PG, pregeniculate nucleus; PL, lateral pulvinar; PM,
medial pulvinar; V1, primary visual area (striate cortex); WGA-HRP, wheat
germ agglutinin conjugated to horseradish peroxidase.
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