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Afferents from the colliculus cortex and retina have distinct terminal morphologies in the lateral posterior thalamic nucleus

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Afferents From the Colliculus, Cortex,
and Retina Have Distinct Terminal
Morphologies in the Lateral Posterior
Thalamic Nucleus
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology,
Cambridge, Massachusetts 02139
We have examined the morphology of afferent endings that originate in three distinct cell
groups and terminate in the lateral posterior nucleus of the thalamus (LP). Retino-LP
projections were sparse, occurred throughout the nucleus, and could be classified into 1)
simple en passant varicosities and terminal swellings found on poorly branched fibers in all
LP subdivisions, 2) string-like configurations of varicosities detected largely in the medial
subdivision of the LP, and 3) terminals resembling retinogeniculate endings occurring mainly
in the rostral part of the superficial subdivision of the LP adjacent to the dorsal nucleus of the
lateral geniculate body. Cortico-LP terminals fell into three classes: 1) single varicosities
decorating the tips of short appendages on fine preterminal and terminal axons; 2) tiny, round
varicosities studding the axon shaft; and 3) boutons of variable shape visible on mediumcaliber corticothalamic fibers. Tecto-LP terminals exhibited a large variation in morphology
and density. Those found most commonly could be classified into two groups: 1) individual
swellings and 2) terminal clusters arranged in a tubular configuration that enclosed a central
channel, most likely occupied by the dendrite of a postsynaptic neuron. An unusual tecto-LP
terminal consisted of an ovoid swelling (up to 20 µm in the long axis) from which emerged
several long, thin extensions and was seen at the tips of large-diameter axons. These results
show that, despite having overlapping projection zones, each set of afferents that projects to
the LP elaborates terminal specializations that are structurally distinct from others projecting to the same target area. J. Comp. Neurol. 388:467–483, 1997. r 1997 Wiley-Liss, Inc.
Indexing terms: axons; presynaptic terminals; rodents; visual pathway; immunocytochemistry
Structure-function relationships form an essential underpinning of nervous system organization (Rouiller et al.,
1986). For some regions of the brain, such as the cerebellum, hippocampus, and retina, the geometric arrangement
of cell bodies, of their dendrites, and of afferent axon
systems that innervate them, is known in considerable
detail. However, for many central nervous system cell
groups, this kind of information is fragmentary at best.
Data compiled from several decades of study (using Golgi
silver-impregnated material, retrogradely labeled neurons, or intracellular fills of single cells) have led to the
successful definition of various cell types, but, for the most
part, the delineation of afferent arbor morphology has
remained refractory in all but the youngest animals. The
recent introduction of anatomical tracers, such as biocytin
or Phaseolus vulgaris-leucoagglutinin (PHA-L), has alleviated this lack to some degree (Gerfen and Sawchenko, 1984;
McDonald, 1992; Aggoun-Zouaoui and Innocenti, 1994;
Bourassa et al., 1994; de Venecia and McMullen, 1994;
Bourassa and Deschenes, 1995; Tamamaki et al., 1995),
but progress in understanding the spatial configuration of
axon arbors and the variations in their terminal specializations has been slow.
In this report, we present observations on the morphological characteristics of afferents that project to the
Grant sponsor: NIH; Grant numbers: EY05504, EY 00126, EY 02621.
Changying Ling is currently at the Center for Neuroscience, University
of Wisconsin, Madison, WI 53706.
David Northmore is currently at the Department of Psychology, University of Delaware, Newark, DE 19716.
*Correspondence to: Dr. Sonal Jhaveri, M.I.T., E25-642a, Cambridge, MA
02139. E-mail:
Received 16 August 1996; Revised 10 June 1997; Accepted 16 June 1997.
lateral posterior nucleus (LP) of the hamster thalamus.
This nucleus receives two major inputs, from the occipital
cortex and from the superior colliculus (SC), in addition to
a direct (albeit minor) innervation from the retina
(Schneider, 1973; Crain and Hall, 1980a–d; BennettClarke et al., 1991). Although the rodent LP has been
studied both at the light and electron microscope levels,
these earlier studies have either focused on delineating the
terminal zones of projections that originate in various
sources or provided an ultrastructural characterization of
their synaptic specializations. Little is known about the
appearance of the afferent arbor or about the way afferent
terminals are clustered together. In this study, we have
used sensitive anterograde tracers (B fragment of cholera
toxin [CT-B], PHA-L, or biotinylated dextrans [BD]) to
label each of three afferent systems that innervate the LP.
We report here that the terminal morphologies of axon
arbors originating in each afferent cell group are distinct.
Their terminal zones are largely overlapping within the
LP, although the density of projection of each afferent
system varies across the subdivisions of the LP. Furthermore, because we were interested in whether there is a
systematic alteration in these terminal specializations
following elimination of one set of afferents during early
postnatal life and the subsequent sprouting of the others
(Ling et al., 1997), the present findings serve as baseline
anatomical observations on normal animals that have not
been available to date for this nucleus.
Data from 78 adult Syrian hamsters (Mesocricetus auratus) of both sexes are included in this study. Animals were
purchased from Charles River Laboratories (Wilmington,
MA) or bred in our colony at Massachusetts Institute of
Technology (M.I.T.) and were maintained in a 14 hour/10
hour light/dark cycle. Each animal was assigned to one of
three groups (see below), was deeply anesthetized with a
combination of sodium pentobarbital (50 mg/kg) and valium
(10 mg/kg), and was placed in a head holder. All protocols
alpha component of the LGBd
central lateral nucleus of the thalamus
lateral nucleus of the thalamus
dorsal nucleus of the lateral geniculate body
ventral nucleus of the lateral geniculate body
lateral posterior nucleus of the thalamus
caudal subdivision of LP
deep subdivision of LP
medialmost subdivision of LP
superficial subdivision of LP
medial geniculate nucleus
nucleus of the optic tract
optic tract
paracentral nucleus of the thalamus
cerebral peduncle
posterior complex of the thalamus
anterior pretectal nucleus
olivary pretectal nucleus
reticular nucleus of the thalamus
superior colliculus
superficial gray layer of the SC
stria medullaris
optic fiber layer of the SC
ventral anterior-ventral lateral nucleus, thalamus
ventrobasal nucleus, thalamus
zona incerta
used with live animals were approved by the Committee
on Animal Care at M.I.T.
Application of tracers
Twenty hamsters in group I received an injection of 1 µl
of CT-B (List Biological Laboratories, Campbell, CA; diluted to 1% in distilled water) into the vitreous chamber of
the left eye via a glass micropipette attached to a microdispenser (Drummond Scientific Co., Broomall, PA). Twentytwo animals in group II received unilateral injections into
the posterior cortex (for location of injection sites, see Fig.
6): Eight of these hamsters received multiple pressure
injections of BD [3 µl of 5% BD (Molecular Probes, Inc.
Eugene, OR) diluted in distilled water] administered via a
glass micropipette (10–15 µm tip diameter) attached to a
microdispenser, two hamsters received multiple injections
of CT-B (3 µl total for each hamster) delivered as for the
BD, and the rest of the animals (n 5 12) were each
subjected to a single iontophoretic injection of PHA-L
[Vector Laboratories, Burlingame, CA; 2.5% solution in
phosphate-buffered saline (PBS) 0.05 M, pH 7.4] through a
glass micropipette (10–15 µm tip diameter). The injection
was made over a period of 15 minutes with a 5-µA positive
current pulsed 7 seconds on, 7 seconds off, by a Midgard
constant-current generator. Finally, 38 hamsters in group
III received unilateral injections of tracers into the SC: For
some of these cases, the visual cortex was suctioned out,
and multiple pressure injections of CT-B (n 5 2) or of BD
(n 5 12) were made into the SC under direct vision. Other
group III animals received iontophoretic deposits of PHA-L
(n 5 24; injection parameters as described above) after
positioning the micropipette (10-µm tip diameter) in the
retinorecipient zone of the SC by physiological guidance:
The pipette was advanced toward the SC while monitoring
the amplified, visually evoked activity, and tracer deposits
were made in the region where strong multiunit activation
was obtained.
Four days after administration of CT-B or 8 days after
BD injection, hamsters were deeply anesthetized by using
sodium pentobarbital and were perfused transcardially
with 0.9% sodium chloride containing 0.25% sodium nitrite as a vasodilator. This was followed by 2% paraformaldehyde in 0.1 M phosphate buffer, pH 7.4 (PB). Animals
that received PHA-L injections survived for up to 10 days
and were then perfused with cold saline containing 0.25%
sodium nitrite followed by 4% paraformaldehyde in 0.1 M
acetate buffer, pH 6.5, then by 4% paraformaldehyde and
0.05% glutaraldehyde in 0.05 M borate buffer, pH 9.5
(details in Gerfen and Sawchenko, 1984). All brains were
cryoprotected in buffered sucrose and were then cut at a
thickness of 40 µm in the coronal plane on a freezing
microtome. Free-floating sections were collected in buffer
and were processed for localization of the tracers.
To visualize CT-B (Mikkelsen, 1992; Angelucci et al.,
1996), tissue was thoroughly washed in PBS and then
immersed sequentially in 0.1 M glycine (made up in PBS)
for 30 minutes; in 2% Triton X-100, 2% normal rabbit
serum (NRS) plus 2.5% bovine serum albumin (BSA) for 1
hour at room temperature; in goat anti-CT-B antibody
(List Biological Laboratories; diluted 1:8,000 in PBS containing 2% Triton X-100, 2% NRS, and 2.5% BSA) for 96
hours at 4°C; in biotinylated rabbit anti-goat secondary
antibody (Vector Laboratories; diluted 1:200 in PBS con-
taining 2% Triton X-100, 2% NRS, and 2.5% BSA) for 90
minutes at room temperature; and in an avidin-biotinperoxidase complex (Elite ABC kit; Vector Laboratories)
for 90 minutes at room temperature. The horseradish
peroxidase (HRP) was visualized histochemically by using
3,38-diaminobenzidine tetrahydrochloride (DAB) as a chromagen, and the reaction product was enhanced with the
addition of 0.02% cobalt acetate. To visualize PHA-L
(Gerfen and Sawchenko, 1984), sections were incubated
overnight at 4°C in PBS containing 0.3% Triton X-100 and
2% NRS; then in goat anti-PHA-L1E antibody (Vector
Laboratories; diluted 1:1,000 in PBS containing 0.3%
Triton X-100 and 2% NRS) for 96 hours at 4°C; then in
rabbit anti-goat biotinylated secondary antibody, followed
by avidin-biotin-HRP, and, finally, the HRP was visualized
with DAB, as described above for the CT-B-labeled sections. To visualize BD (Rajakumar et al., 1993), tissue was
reacted directly with avidin-biotin-peroxidase complex
(Elite ABC kit; Vector Laboratories; diluted 1:100 in PB)
for 90 minutes at room temperature. After washing thoroughly, sections were reacted with DAB, as described
All sections were mounted on chrome alum- and gelatincoated slides, air dried, dehydrated, and coverslipped.
Tissue was analyzed under the microscope at both low
(3100) and high (31,000) magnification and was photographed, or axons were drawn with the aid of a drawing
tube attachment.
Subdividing LP
The cytoarchitecture and fiber architecture of the hamster LP was examined in sections from our laboratory
collection of normal adult brain sections processed with
silver stains (Schneider, 1969) for viewing normal fibers,
with the Loyez stain for the distribution of myelinated
axons, and with cresyl violet for studying the distribution
of cell bodies. In addition, borders of individual subdivisions were also determined on the basis of hodological
observations for this region (Schneider, 1969, 1973, 1975;
Lent, 1982; Jhaveri et al., 1985; Ling et al., unpublished
Architecture of the hamster LP
Our subdivisions of the hamster LP are slightly different
(see Fig. 1) from those described by Crain and Hall
(1980a). We defined a superficial subdivision, referred to
as LP-s, that was characterized by lighter neuropil than in
the rest of the nucleus, as seen in fiber stains. This region
received very dense projections from the superficial layers
of the SC. At caudal levels of the nucleus, LP-s extended
from the edge of the LGBd (laterally) to the pretectum
(medially), whereas, in more rostral sections, LP-s was
abutted medially by the dorsal extension of the deep
subdivision (LP-d), which reaches the diencephalic surface
at this level. In normal fiber stains, LP-d had a denser
neuropil, and, through it, traveled many corticofugal fibers
of passage destined for pretectal and tectal targets. In
silver-degeneration material, LP-d was seen to receive
input from deeper tectal layers as well as from visual
cortex. Although LP-s and LP-d are fairly similar in extent
to what Crain and Hall call LP-rl and LP-rm, we prefer the
‘‘superficial’’ and ‘‘deep’’ nomenclature, because it allows
orientation of the subdivisions relative to the optic tract;
see Discussion. At rostral levels in the hamster, the a
subdivision of the LGBd was seen to be continuous with
LP-d. At most levels of the LP, an additional, medial-most
region of lighter neuropil was evident; we designated it as
LP-m. In sections immunostained with an antibody against
GAP-43, this subdivision stands out by virtue of its denser
immunoreactivity (Moya et al., 1990; Schneider and Benowitz, unpublished observation). In some sections, this lighter
neuropil extended more superficially, but such a delineation was not seen consistently, and is not illustrated in
Figure 1. Caudally, LP-d extended into a region of dense
fibers: This subdivision was referred to as LP-c by Crain
and Hall (1980a) and likewise by us (however, see Discussion). In Nissl stains, these subdivisions were difficult to
differentiate in the hamster. Ventral to LP-d, the boundary
with the underlying posterior or ventral thalamic nuclei
was not a sharp one. It was drawn by convention along the
course of the external medullary lamina, although some
projections from the tectum did extend below this line.
Morphological specializations
of retino-LP projections
Injections of CT-B into the vitreous chamber of the eye
result in uptake and anterograde transport of the tracer by
retinal ganglion cells. CT-B-labeled axons were observed
in all known retinorecipient zones, and sparse, labeled
fibers were also revealed in some regions of the brain that
have not been recognized previously as targets for primary
visual afferents (Ling et al., 1994). Earlier reports have
documented that a restricted portion of LP-s adjacent to
the superficial optic tract receives a small focus of contralaterally projecting retinal fibers (Schneider, 1973; Crain
and Hall, 1980a). Labeling with CT-B revealed that, in
addition to these tiny foci, scattered retinal terminals were
also present throughout much of the rest of the LP;
however, the density of the retino-LP projection was
higher in the LP-s at rostral levels (Fig. 2a) and in the
LP-m at central levels of the nucleus (Fig. 2b).
Retinal axons that entered the LP left the main optic
tract just below the ventral nucleus of the lateral geniculate body (LGBv) and followed a deeper trajectory through
the parenchyma of the LGBv and LGBd, contributing to
fibers of the internal optic tract (IOT; Schneider and
Jhaveri, 1983). These axons penetrated the LP across its
border with the LGBd and, for the most part, were bundled
into distinct fascicles that coursed parallel to the surface of
the dorsolateral thalamus (Fig. 2a). (It is possible that
some retinal axon collaterals also entered the nucleus
directly from the superficial optic tract; such a collateralization, if it did occur, would be difficult to detect in our
material because of the dense labeling of surface optic
tract axons.) Most retinal fibers that passed through the
LP exhibited sparse ramification, and their terminal specializations could be classified into three groups.
Varicosities and simple endings on individual collaterals. A scattered distribution of fine fiber collaterals
was noted emerging from retinal axons as they coursed
through the LP. These afferents bore en passant swellings
of various sizes: tiny (,1 µm in diameter; Fig. 3a), small
(1–2 µm in diameter; Fig. 3b), and medium-sized (.2 µm
in diameter; Fig. 3c) varicosities were loosely strung along
the length of the fiber collaterals. A simple terminal bouton
was often noted at the end of each collateral of the
preterminal axon (Fig. 3, arrowheads). No specific clustering of these swellings was apparent. Such ramifications
Fig. 1. Top: Schematic diagram illustrating the subdivisions of the
lateral posterior nucleus (LP) in a series of frontal sections taken at
rostral (left), middle, and caudal (right) levels of the nucleus. The
superficial subdivision (LP-s), deep subdivision (LP-d), medial subdivision (LP-m), and caudal subdivision (LP-c) are indicated. At caudal
levels of the nucleus, LP-s extends from the edge of the dorsal nucleus
of the lateral geniculate body (LGBd; laterally) to the pretectum
(medially), whereas, in more rostral sections, it is abutted medially by
the dorsal extension of LP-d. LP-d is continuous with the alpha (a)
subdivision of LGBd at rostral levels and is replaced by LP-c at caudal
levels of the nucleus. LP-m forms the medialmost subdivision and is
visible at most levels. Bottom: Photomicrographs from silver-stained
frontal sections through the LP showing the fiber architecture through
the nucleus in relation to its subdivisions. The orientation and level of
each section is indicated by the gray box in the corresponding
schematic diagram above each section. For abbreviations, see list.
Scale bar 5 1,000 µm for top, 200 µm for bottom.
were found in all subdivisions of the LP, with a slightly
higher density in LP-m at central levels of the nucleus
(Fig. 2b).
String-like complexes. These were found primarily in
LP-m at midlevels of the nucleus (Fig. 2b), and their
distribution overlapped that of the simple endings described above. Each complex was comprised of several (at
least two) individual fibers that were studded with boutons of various sizes, primarily of the small and medium
category (Fig. 4). The swellings occurred closer together
than the simple endings described above. A longitudinal
arrangement of such bouton-studded fiber strings could
frequently be visualized in which two or more fibers
traveled together for a distance and then separated (Fig. 4).
Terminals resembling normal retinogeniculate endings. Previous studies (Erzurumlu et al., 1988) have
identified at least two distinct types of retinal terminals in
the LGBd (labeled terminals shown in Fig. 5a–d are from
the LGBd). Type R1 terminals consist of large, oval
swellings that are strung along thick axons (Fig. 5a),
whereas type R2 terminals are comprised of rosette-like
clusters of small or medium varicosities that emerge from
fine-caliber retinal afferents (Fig. 5b–d). In general, more
than one afferent collateral contributes to each cluster of
R2s (Fig. 5c,d). (Ubiquitous type R3 retinogeniculate terminals are comprised of endings that do not fall into the type
R1 or type R2 categories, and they are not discussed here.)
Both of these classes of endings could be identified in the
LP: Terminals with morphologies typical of type R1 (Fig.
5e,f) and R2 retinogeniculate endings (Fig. 5g–j) were
found primarily in LP-s at rostral levels. They were
present near the border of the LP and LGBd but were
distinctly outside the latter cell group, in a region designated as the retinorecipient zone of the LP in earlier
studies (Schneider, 1973; Crain and Hall, 1980a).
Terminals of visual cortico-LP afferents
The rodent visual cortex is comprised of three distinct
architectonic fields (Fig. 6): striate cortex or area 17 and a
peristriate ‘‘belt’’ formed by area 18a laterally and 18b
medially (Schneider, 1969; Caviness, 1975; Tiao and Blakemore, 1976a,b; Lent, 1982; Olavarria and Van Sluyters,
1985; Rhoades et al., 1987; Lewis and Olavarria, 1995). In
Fig. 2. Photomicrographs of frontal sections through the LP of
adult hamsters that had injections of cholera toxin in the contralateral
eye (a,b), of Phaseolus vulgaris-leucoagglutinin (PHA-L) in the ipsilateral visual cortex (c), and of PHA-L in the ipsilateral superior
colliculus (d). These views indicate the relative densities and distributions of inputs from these three cell groups. In a and b, sparse
retino-LP terminals extend from optic axons that run through the
nucleus parallel to the surface of the thalamus. Retino-LP terminals
have a relatively high density in LP-s at rostral levels (a) and in LP-m
at mid-LP levels (b). In c, cortico-LP projections at mid-LP levels have
a high density in LP-d, whereas, in d, tecto-LP projections at mid-LP
levels show a dense projection in LP-s. Arrowheads point to the border
between the LP and LGBd in each micrograph. For abbreviations, see
list. Scale bar 5 50 µm in a, 100 µm in b–d.
our study, cortical injections were largely restricted to area
17 (for the location of the centers of injection sites, see Fig.
6). Each deposit of tracer (PHA-L, CT-B, or BD) resulted in
a cylindrical-shaped region of labeled cells and processes
approximately 0.6–1.0 mm in diameter and 0.6–1.0 mm in
depth. The injection site extended through most or all
cortical layers (see Fig. 7 for typical injection site). CT-B
and BD were transported both anterogradely and retrogradely, whereas only anterogradely filled axonal profiles
that projected to the LP were seen following iontophoretic
injections of PHA-L. Results that were confirmed with all
three methods are described here, with photographic
documentation derived from the PHA-L-labeled tissue.
Labeled corticofugal fibers en route to the LP coursed
largely in the external medullary lamina, peeling off
laterally to innervate target cells. Terminal arbors of
cortico-LP axons were observed throughout the LP on the
side of the injection, including the LP-s, a region that also
receives a dense projection from the SC (Fig. 2c; see below).
On morphological grounds, cortico-LP terminals could be
classified into three types. The first two types occurred on
fine fibers (diameter 1 µm or less), which constituted the
majority of cortical arbors. They bore tiny, round varicosities (diameter ,1–1.5 µm; Figs. 8, 9), and the density of
short branches and spine-like appendages varied signifi-
cantly from one fiber to the next (Figs. 8, 9a–c). According
to the morphological characterization by Bourassa and
Deschenes (1995) for cortico-LP axons in the rat, these
fibers could be divided into two groups: 1) Type I afferents
were branched and bore numerous short appendages (Fig.
8, arrow, Fig. 9c), and 2) type II fibers were less heavily
branched but were studded with varicosities along the
length of the shaft or at the tip of the ramification (Fig. 8,
arrowhead, Fig. 9a). Although some labeled fibers could be
classified as belonging to one or the other of these types,
intermediate forms, like that shown in Figure 9b, were
also seen. Thus, in the hamster, these two groups of fibers
may represent extreme variations within a single category
(see Discussion). Long lengths (up to 200 µm) of preterminal arbors could be traced in 40-µm-thick coronal sections,
suggesting that these arbor ramifications occurred primarily in the transverse plane (Fig. 8). 3) In addition, a less
frequently seen fiber type (type III) consisted of mediumsized axons (,2 µm diameter). Type III fibers bore mediumsized varicosities (3–4 µm diameter; Fig. 9d,e) that had a
sparser distribution along the length of axons. Although
points of bifurcation could be detected (Fig. 9e, arrows), by
and large these axons appeared to be unbranched within
the LP. The projection zones of the three types of cortico-LP
Fig. 3. Photomicrographs showing higher magnification views of cholera toxin-labeled varicosities
and simple endings on individual retino-LP axon collaterals. a: Tiny boutons (,1 µm average diameter).
b: Small boutons (1–2 µm average diameter). c: Medium boutons (.2 µm average diameter). Arrowheads
point to terminal boutons. Scale bar 5 10 µm.
Fig. 4. Photomicrographs showing the detailed morphology of string-like complexes formed by cholera
toxin-labeled retinal axons in LP. Each complex is comprised of segments of more than two collaterals that
are densely studded with boutons of small (a), medium (b,c), and tiny (d) size. Scale bar 5 10 µm.
arbors were largely overlapping (Figs. 8, 9d). At a qualitative level, fiber types I and II, bearing tiny varicosities,
predominated in most regions of the LP, with fewer
medium-sized axons bearing simple varicosities. This was
true even in the anterolateral corner of the LP-d, where
the heaviest density of medium-sized cortical afferents
was seen.
Terminals of tecto-LP afferents
In most of our cases, tracer injections were restricted to
the upper half of the SC, including the superficial gray
(SGS), the optic fiber layer (SO), and the intermediate gray
layer (a typical injection site is shown in Fig. 7b), although,
in a few (less than 1⁄3) cases, injection sites also encroached
Fig. 5. Detailed morphology of type R1 and type R2 retinogeniculate terminals (a–d), and type R1- and type R2-like retino-LP terminals (e–j) seen in animals in which retinal axons are labeled with the B
fragment of cholera toxin (CT-B). In the dorsal nucleus of the lateral
geniculate body (LGBd), type R1 terminals form large, ovoid boutons
Fig. 6. Schematic diagram representing a dorsal view of the caudal
portion of the hamster brain indicating the center of placement of
PHA-L (circles), biotinylated dextran (black dots), and cholera toxin
(gray dots) injections on the right side in relation to subdivisions of the
occipital cortex, which are delineated on the left side (17, cortical area
17 or striate cortex; 18a, cortical area 18a or lateral juxtastriate
cortex; 18; cortical area 18, medial juxtastriate cortex or cortical area
18b). Scale bar 5 1,500 µm.
upon deeper layers, including the dorsal edge of the central
gray. With all three tracers, the same colliculo-LP terminal
types were identified, and no retrogradely labeled cells
that are loosely strung along thick fibers (a), whereas type R2
terminals consist of medium- and small-sized boutons that form
rosette-like clusters and that emerge from fine-caliber axons (b–d).
R1-like retino-LP terminals (e,f) and R2-like retino-LP terminals (g–j)
resemble the endings in the LGBd. Scale bar 5 10 µm.
were seen in the LP (the LP does not normally project to
the tectum). No attempt was made in this study to
separate terminal types according to whether they originated in the SGS, SO, or deeper layers (earlier studies
have shown that tecto-LP projections originate largely
from the lower portion of the SGS and the SO; albino rat:
Sugita et al., 1983; other mammals: for review, see Huerta
and Harting, 1984; hamster: Mooney et al., 1988; BennettClarke et al., 1991).
Our results showed that the SC projects bilaterally to
the LP, with the ipsilateral pathway being by far the
predominant one. Tectal afferents to the ipsilateral LP
entered the nucleus through the parenchyma of the lateral
pretectum or via the brachium of the SC, whereas axons
that projected contralaterally crossed in the postoptic
commissure and ascended within the opposite optic tract.
On the ipsilateral side, the highest density of tectal
projections occurred in the LP-s (Fig. 2d), but labeled
afferents were also found throughout the rest of this
thalamic target. There was a large variation in the morphology of tecto-LP terminals, but the most commonly seen
endings could be grouped into two types: 1) Individual
terminals were found on fibers that had an average
diameter of about 1 µm. These afferents were smooth for
the most part and bore a sparse distribution of swellings
that varied in diameter from 1.5 to 4 µm. The majority of
such swellings were detected on short appendages that
decorated axon trunks; some were located at the tip of a
Fig. 8. Photomicrographs of PHA-L-labeled cortico-LP afferents.
The majority of cortico-LP projections are formed by fine-caliber axons
bearing tiny, round varicosities. Many of the boutons on these axons
decorate the tips of short appendages along the length of the fiber (type
I axon, arrow; see also Fig. 9), but varicosities are also present along
the length of the axon shaft (type II axons, arrowhead). Considerable
variation in the density of varicosities is seen from one collateral to the
next. Scale bar 5 25 µm.
Fig. 7. Photomicrographs illustrating typical injection sites in area
17 (a) and in the superior colliculus (SC; b). Arrow in a indicates the
ventral border of layer VI. In both cases illustrated here, the tracer
used was PHA-L. Dashed line in b indicates the border between the
superficial gray layer of the SC and the optic fiber layer; arrow
indicates the tectal midline (b). Scale bar 5 500 µm.
terminal branch (Fig. 10). Occasionally, several collaterals
bearing these types of endings were seen to form loose
clusters (Fig. 10, long arrows). These individual terminals
were morphologically distinct from the simple endings on
retino-LP afferents by virtue of their more frequent branching and by the presence of short appendages along the
axon shaft (Fig. 10, short arrows). 2) Tubular clusters of
tecto-LP terminals were each comprised of 20–40 boutons
aligned around a central, cylindrical channel that was
approximately 1–3 µm in diameter and up to 20–30 µm in
length (Fig. 11b,c, arrows). Boutons within each cluster
were so closely aggregated at times that it was difficult to
delineate individual swellings (Fig. 11a,d, arrows). The
central channel had a size and shape consistent with the
possibility that it was occupied by the dendrite of a
postsynaptic neuron (see Discussion). The average outer
diameter for a single tubular cluster was about 4–6 µm.
Other groups of boutons, which may or may not have
surrounded a central cavity of a similar dimension, formed
a round or ovoid (rather than longitudinal) arrangement
(Fig. 11, arrowheads). We assume these arose as a result of
transverse or oblique sections through the tubular clusters. Whereas the individual endings had a dense distribution, the tubular clusters were more visually striking
because of their distinctive morphology (Fig. 2d). In addition to the two types of tecto-LP endings described above, a
third, infrequently seen terminal occurred on largediameter (2–4 µm) axons and had a unique morphology. It
consisted of a large, ovoid terminal swelling (up to 20 µm)
at the axon tip from which emerged several long, thin
extensions (Fig. 12). Terminals with this kind of morphol-
ogy could also be smaller in size and occurred on thinner
The density of the different tectal efferents varied in
different regions of the LP, but both of the commonly seen
types of terminals of axons from SC were present throughout this target, including the LP-d, the region that was
previously believed to receive a projection only from visual
cortex (LP-rm in Crain and Hall, 1980a). The distribution
of the various classes of tecto-LP endings was largely
overlapping. The highest density of tecto-LP projections
occurred in the LP-s, a region that also received a moderate projection from the contralateral SC and from the
ipsilateral visual cortex (area 17), in addition to a sparse
projection from the contralateral retina (Fig. 13). Labeled
terminal profiles shown in Figures 3–5 and 8–11 were
derived primarily from this region. (In Fig. 4, the stringlike complexes of retinal origin shown are in the LP-m.)
The LP (or portions of the pulvinar of cats and monkeys)
is known to participate in an extrageniculate visual pathway that links the SC and the pretectum to visual cortex in
mammals (Diamond, 1973; Graybiel and Berson, 1980,
1981). It is also widely accepted that the LP receives inputs
at least from the SC, the visual cortex, and the retina and
that it sends afferents to the visual cortex (Nauta and
Bucher, 1954; Abplanalp, 1970; Benevento and Ebner,
1970; Harting et al., 1973; Karamanlidis and Giolli, 1977;
Robson and Hall, 1977a,b; Arango and Scalia, 1978; Gould
et al., 1978; Dursteler et al., 1979; Hollander et al., 1979;
Karamanlidis et al., 1979; Caviness and Frost, 1980;
Coleman and Clerici, 1980, 1981; Crain and Hall, 1980a;
Perry, 1980; Linden and Rocha-Miranda, 1981; Raczkowski and Diamond, 1981; Lent, 1982). A considerable
amount of information is available about the distribution
Fig. 9. Detailed morphology of cortico-LP terminals. The column
on the left (b–e) shows camera lucida drawings of axons from the
corresponding photomicrographs in the right column. a: Type II axon
with varicosities primarily along the axon shaft. b: Axon arbor with
morphology that is of a form intermediate between type I and type II
axons. c: Type I axon arbor—note the numerous short appendages
studded with tiny varicosities. d: Illustration of the overlapping
distribution of the various terminal types. e: Type III axon arbors;
arrows indicate points of bifurcation on the type III arbors. Scale
bar 5 10 µm.
major input from the external nucleus of the inferior
colliculus (unpublished data) and could just as well be
considered to be part of the medial geniculate body, as has
been noted for rats (LeDoux et al., 1985; GonzalezHernandez et al., 1991).
In terms of projection zones, our observations confirm
and extend those of Crain and Hall. We show that afferents
to the LP have a significantly more widespread projection
zone than was detected previously and that the overall
zones of termination from the retina, SC, and visual cortex
are overlapping, including in the LP-d (Fig. 2), a region
that was thought previously to receive only visual cortical
afferents. However, the relative density of each afferent
system varies within the subdivisions of the LP (Fig. 13).
Differences between our results and those of Crain and
Hall are most likely due to the greater sensitivity of the
anterograde tracers we have employed for this study and
the greater facility for detailed sampling over the entire
nucleus with the light microscope. Furthermore, staining
for degenerating axons or using 3H-amino acid autoradiography results in a discontinuous labeling of axons, with
varying levels of background staining. Thus, with these
older tracing techniques, it would have been difficult to
differentiate a sparse terminal projection (such as that
from the retina to the LP) from labeled axons of passage. In
the present study, we have used several different tracers,
each of which provides a diffuse fill of preterminal axons
and their terminal arbors, making it easier to distinguish
sparse terminal specializations from axons that are passing through the target region.
Differential morphological specification
of afferent arbors from different sources
Fig. 10. Camera lucida drawings of individual tecto-LP terminals.
These endings are of various sizes, are sparsely distributed, and are
seen on fine-caliber axons. Long arrows, loose bouton clusters; short
arrows, short appendages along axon shafts. Scale bar 5 10 µm.
and ultrastructural characteristics of LP terminals that
derive from different sources. Despite the large volume of
anatomical work devoted to the study of this nucleus, the
present results are novel in providing light microscopic
information on the morphology of terminal specializations
on afferents arising from the retina, cortex, or tectum and
projecting to the LP.
Overlapping terminal fields of axons
from different sources
Crain and Hall (1980a) delineate three subdivisions of
the hamster LP, basing their conclusions on cytoarchitectonic and myeloarchitectonic criteria and on a description
of the projection pattern of retino-LP, cortical-LP, and
tecto-LP afferents to each of these subdivisions. Our
subdivisions agree in part with this earlier definition, but
we have modified the borders slightly on the basis of
additional data from normal fiber stains and from hodological studies. First, to simplify the nomenclature, we have
referred to the two major subdivisions as superficial and
deep in relation to the optic tract. Thus, our LP-s is
essentially the same as LP-rl of Crain and Hall (1980a). In
addition, primarily on the basis of normal fiber architecture, we have distinguished a medial subdivision (LP-m)
that was not delineated in the earlier study. Our definition
of the borders of the LP-c agree with those of Crain and
Hall, but we point out that the hampster LP-c receives a
Our results document the morphology of afferent arbors
in the LP, with a special focus on the form and clustering of
terminal endings, and they provide a perspective that is
not generally possible to obtain from ultrastructural observations. We show that afferent arbors and terminals in this
nucleus display source-specific features that differentiate
them from other afferents projecting to the same zones.
Afferents from the retina. Retinal axons headed toward the SC follow one of two routes: Most of them course
along the diencephalic surface in the superficial optic
tract. However, at the ventral edge of the LGBv, significant
numbers of retinal axons diverge from the surface fibers
and enter the internal optic tract (Schneider and Jhaveri,
1983; Bhide and Frost, 1991). These fibers course through
the parenchyma of the LGBv, LGBd, and LP on their way
to caudal targets. In earlier studies that used degeneration
techniques (or anterograde transport of 3H-amino acid, or
HRP) to label retinal axons, it was concluded that, with the
exception of a few tiny foci of terminals, most of the labeled
retinal axons in the LP were merely passing through, and
there was virtually no direct retino-LP projection
(Schneider, 1973; Crain and Hall, 1980a). An exception to
this was thought to occur during development (Perry and
Cowey, 1982). It was argued on the basis of HRP labeling
that there could exist a transient retino-LP projection that
gets eliminated during early postnatal life. Those authors
suggested that the abnormal retinal projection to the LP
that forms after early ablations of the tectum (Schneider,
1973) results from an arrest of this elimination process.
Although irrevocable evidence for such a transient
retino-LP projection during development has not been
forthcoming, the use of CT-B to label retinal axons in the
Fig. 11. a–f: Photomicrographs (a,c–f) and camera lucida drawings
(b) showing the morphology of tecto-LP terminals that form tubular
clusters. A typical tubular cluster (arrows) is comprised of 20–40
boutons, which form an array that can extend up to 30–40 µm in
length and which are aligned around a central channel (1–3 µm in
diameter). Other boutonal clusters (arrowheads) form round or ovoid
configurations and also surround a central cavity of a similar dimension—these are most likely cross-sections through the tubular clusters. Because of the dense packing of the terminals, some individual
varicosities are not clearly visualized (a,d). Scale bar 5 10 µm.
Fig. 12. Camera lucida drawings (top) and photomicrograph (bottom) of PHA-L-labeled superior colliculus (SC)-LP terminals found on
large-caliber fibers. The endings consist of a large ovoid swelling at the
axon tip with several long, thin extensions emerging from it. Such
endings are infrequently seen in the tecto-LP projection. Scale
bar 5 10 µm.
developing animal may yet provide the definitive answer.
Clearly, in the adult, varicosities are visible on retinal
fibers as they course through the LP. However, it is not
known whether some of these specializations form on
axons that are collaterals of fibers that go on to other
targets or whether they are retinal axons that are destined
specifically for the LP. The close resemblance between type
R1 and type R2 retinal terminals in the LGBd and those in
the LP might suggest that some retino-LP axons are a
continuation of retino-LGBd afferents. In any case, our
observations clearly document that terminal and preterminal specializations on retinal axons are scattered throughout the LP and are not restricted to the tiny, dense foci
described in the prior studies. Although, overall, this
projection is relatively minor, the widespread nature of
optic afferents in most LP subdivisions is relevant to the
distribution of sprouted retino-LP terminals that occur
following early tectal lesions (see Ling et al., 1997).
Ultrastructural correlates of the swellings and terminal
specializations we illustrate here remain unclear. Only one
type of synaptic bouton, the RS terminal, has been described in the LP as deriving from the retina. However, on
the basis of size and clustering, it is not possible to assign
the RS terminal to any one of the retino-LP specializations
that we have observed in this study. Our type R1 endings
are too large, and one would expect most of the type R2
endings to be clustered in the EM, as they are in the LGBd
(Szentagothai, 1963; Szentagothai et al., 1966; Guillery,
1969; Guillery and Scott, 1971; Famiglietti and Peters,
1972; Lund and Cunningham 1972; Rafols and Valverde,
1973); with regard to the swellings that are on the
string-like complexes or that comprise the simple endings
on individual collaterals, these varicosities exhibit a substantial variation in size, and they cannot be allotted
unequivocally to correspondence with the RS terminals at
the ultrastructural level. Thus, our data indicate that a
more detailed ultrastructural study of the LP, perhaps in
combination with CT-B labeling of retinal afferents, is
necessary to understand how and where the retinal terminals contact postsynaptic targets in the LP.
Afferents from the SC. The photographic documentation of the tecto-LP axon terminals shown in the present
study was derived from material labeled with PHA-L, but
it was confirmed in cases wherein BD was also used as the
anterograde tracer. There is considerable evidence that
PHA-L is transported long distances along axons in the
anterograde direction (see, e.g., Gerfen and Sawchenko,
1984, 1985; Carlson and Heimer, 1986; Grove et al., 1986;
Rockland et al., 1995). However, the possibility that at
least some of the labeled profiles we see result from
retrograde transport of retinotectal axons and the possibility that our observations are confounded by the labeling of
collateral branches of these back-filled cells into LP must
be considered. Complete labeling of neuronal cell bodies
and dendrites was detected after PHA-L injections, but
only in the region of the injection site. In addition, longdistance retrograde labeling by PHA-L is occasionally
reported, but the labeling density is usually conspicuously
weaker, and the reaction product is granular, not diffuse as
shown in our material (Kita and Kitai, 1987; Lee et al.,
1988; Shu and Peterson, 1988; Clarke et al., 1993). Furthermore, such labeling is reportedly obtained with the use of
larger pipette tips for making the iontophoretic injections
than those used in this study or when making tracer
deposits with pressure injections rather than electrophoretically, as we have done (Gerfen and Sawchenko, 1984,
1985). Based on these considerations, we are confident
that the labeled terminals shown in this study result from
anterograde transport of the tracer.
A tecto-LP projection has been identified in a wide
variety of mammals (Altman and Carpenter, 1961; Morest,
1965; Tarlov and Moore, 1966; Martin, 1969; Abplanalp,
1970; Hall and Ebner, 1970; Niimi et al., 1970; Rafols and
Matzke, 1970; Mathers, 1971; Casagrande et al., 1972;
Graybiel, 1972; Harting et al., 1973; Benevento and Fallon, 1975; Glendenning et al., 1975; Mooney et al., 1988).
Although there are notable variations in the relative size
and subdivisions of the LP among different species, there
are also many similarities. In general, tecto-LP projections
arise largely from the superficial, retinorecipient layers of
Fig. 13. Schematic diagram summarizing the results on the density and distribution of the three systems of afferent arbors that
originate from different sources and terminate in the LP. Retino-LP
terminals: dots, type R1-like and type R2-like terminals; bars, stringlike configurations of retino-LP terminals; squares, varicosities and
simple endings on retino-LP collaterals. Cortico-LP terminals: small
squares, type I and II arbors; large squares: type III arbors. SC-LP
terminals: bars, tubular clusters; circles, individual terminals. For
abbreviation, see list.
the SC, with ipsilateral afferents predominating. Ultrastructural study of tecto-LP terminals reveals three types
of synaptic endings, referred to as M terminals, RS termi-
nals, and F terminals (Robson and Hall, 1977a; Crain and
Hall, 1980a). In hamsters, the majority of tecto-LP axon
arbors form M terminals, which are of medium size,
contain round vesicles, and are generally found tightly
packed together around the shaft of a large proximal
dendrite of a postsynaptic neuron. To a lesser extent, tectal
afferents also form RS and F terminals in the LP: RS
terminals are small sized (,1 µm in diameter), contain
round vesicles, generally synapse on the shaft of a small
dendrite, and are located outside the large synaptic clusters dominated by the M terminals. F terminals, so called
because of their flattened or pleomorphic synaptic vesicles,
are intermediate in size between the M and RS terminals
and infrequently participate in the large synaptic clusters.
Our light microscopic observations on tecto-LP projections can be partially correlated with these ultrastructural
data. Most likely, the M terminals described by Crain and
Hall are the ultrastructural equivalent of what we refer to
as the tubular clusters that surround a central channel—
swellings that comprise these clusters are of a size that
corresponds well with that of the medium-sized M terminals. In the electron microscope (EM), boutons of M
terminals are seen closely abutted to each other, which
could explain why, in some of our examples of tecto-LP
clusters, individual varicosities could not be delineated at
the level of the light microscope (see Fig. 11). The average
outer diameter for a tubular cluster in our material was
about 4–6 µm, the same as that measured for clusters of M
terminals in the figures of Crain and Hall (see, e.g., Fig. 6
in Crain and Hall, 1980a). The tubular conformation of
these clusters is consistent with the hypothesis that the
endings are closely aligned along the proximal dendrites of
LP neurons. Variations in size of the simple endings that
we describe here make it possible that at least some of
them correspond to the RS terminals of Crain and Hall.
However, if size was the only criterion, then the simple
endings most closely match the category of terminals
referred to as the F terminals.
Nonetheless, it should be underscored that the tecto-LP
projection is complex, and we have described here the
morphology of only the most commonly found endings.
Regarding the large endings with trailing processes (Fig.
12), no EM equivalent of these has been reported in the
literature; however, they are rare enough, and one explanation for such an omission might be the difficulty of obtaining a thorough ultrastructural sampling in all parts of the
nucleus. These terminals bear similarities to large endings
in the medial nucleus of the trapezoid body (cf. Morest,
1968, 1975).
Projections from the visual cortex. It has been documented for many mammalian species that the LP receives
a major projection from the ipsilateral visual cortex,
including area 17, and has a reciprocal projection back to
the visual cortex (Updyke, 1975; Robson and Hall, 1977a,b;
Giolli et al., 1978; Ogren and Hendrickson, 1979; Crain
and Hall, 1980a; Lent, 1982; Jones, 1985; Klein et al.,
1986; Bourassa and Deschenes, 1995). In the rat, terminals of cortico-LP axons are of at least two types and likely
originate in neurons of cortical lamina V as well as lamina
VI (Bourassa and Deschenes, 1995).
In hamsters, morphologically distinct cortico-LP synapses have been described previously at the ultrastructural level: 1) RL terminals are large (.2-µm-long axis),
contain round vesicles, and synapse on appendages of
proximal dendrites of LP neurons; they do not show a
tendency to form clusters. RS and F terminals have the
same characteristics as those described for the tecto-LP
projection (Crain and Hall, 1980a). Our light microscope
characterization of cortico-LP terminals showed that the
majority of them were tiny, round varicosities (1–1.5 µm in
diameter; Fig. 9a–d) located along the shaft of fine axons,
but they were also found on the tips of short appendages
that emerged more or less perpendicularly from the parent
axon. Less frequently, medium-sized boutons (3–4 µm
diameter; Fig. 9d,e) were found that had a sparser distribution along the length of medium axons. The larger size of
the RL terminals precludes them from corresponding to
the tiny swellings we have observed on cortico-LP arbors;
this suggests that the medium-sized cortico-LP endings
would be candidates for the light microscope correlate of
the RL terminals. 2) On the other hand, the most common
of cortico-LP terminals, those on the spiny fibers, match
the description of the RS terminals of Crain and Hall
(1980a) on the basis of size alone. However, there is a
discrepancy between their study and ours, in that we find
that the tiny endings on fine fibers are the most commonly
labeled cortico-LP terminals, whereas, in the EM, the
majority of cortico-LP terminals seen are of the RL variety
(and size considerations disallow any correspondence between the tiny varicosities and the RL terminals). One
possibility is that the difference in the two studies arises
from variations in the involvement of lamina V vs. lamina
VI of the cortex at the injection site (see Bourassa and
Deschenes, 1995). In addition, we have attempted to
restrict our injection sites to area 17, whereas, in the
earlier study, tracer applications spread also into area 18
and posterior temporal cortex (Crain and Hall, 1980a).
Thus, many of the RL terminals described in the EM work
might originate in the cortex outside of area 17. However,
it should be underscored that attempts at making such
correlations between light microscopic and ultrastructural
observations, including the ones discussed above, are
confounded; thus, in the EM work, only swellings that
have synaptic vesicles associated with membrane specializations are ascribed to specific terminal classifications,
whereas no differentiation between swellings that do or do
not make synaptic connections is possible in the light
microscope observations.
Bourassa and Deschenes (1995) injected cells in cortical
lamina V or lamina VI, traced the projections to LP, and
found that the terminal ramifications of axons from each
lamina were distinct: All corticothalamic fibers in their
study were of fine caliber (,1.5 µm), those emerging from
lamina VI exhibited en passant swellings (size #1µm) and
tiny varicosities at the tips of short stalks, whereas those
that issued from lamina V also bore swellings, but, on
average, these were slightly larger (,2 µm), and the
majority of them appeared en passant or at the ends of
terminal ramifications. However, note that, although their
layer V afferent endings were different in size from the
type I (layer VI) endings, the difference was slight. In our
study of the hamster, we did not specifically differentiate
between the laminar origins of cortical afferents to the LP;
however, we were unable to group our reconstructed axons
according to a strictly dual classification, as reported for
the rat (Bourassa and Deschenes, 1995). Moreover, fibers
with only en passant swellings and no short appendages,
similar to the type II endings described by Bourassa and
Deschenes for the rat, are present, but infrequently so, in
our material. Finally, in the rat, there appears to be no
cortico-LP axon terminal that resembles the medium-sized
ending we document for the hamster. Overall, our results
show that, instead of the cortical input to the LP being the
‘‘primary’’ one, it is the tectal projections that have a
massive presence throughout much of this nucleus, and
these are likely to have the greatest influence in activation
of LP neurons [cf. Guillery’s (1995) scheme for connectional relationships of first-order and higher order thalamic nuclei]. Additional comparative studies, including
ultrastructural observations, are necessary to resolve these
discrepancies in results or even to show definitively that
these observations might reflect a species-derived difference in the morphology of cortico-LP projections.
We have illustrated the morphology of preterminal and
terminal axons in the LP, and we have documented a
source-specific configuration of the terminal specializations of each afferent system. Although we remain ignorant of the precise significance of these morphological
features, it is clear that only by understanding each set of
projections at both the light microscopic and the EM level
can we hope to uncover structure-function relationships in
groups of cells in the central nervous system. For instance,
it is likely that the tubular clusters formed by tecto-LP
axons represent a highly reliable mode for the transmission of signals between tectal neurons and LP cells (cf.
Rouiller et al., 1986), whereas the spiny fibers, which
derive from the cortex and which bear tiny varicosities at
the tips of their multiple appendages, form an anatomical
substrate for a very different type of signaling (Guillery,
The overlapping distribution within the target, together
with the unique terminal configurations of afferent endings in the LP, could indicate a predominant influence of
the presynaptic neuron in controlling the terminal morphology of axons from different sources. However, such a
conclusion would be somewhat premature at this time,
because we do not know the detailed relationships between
afferent endings and specific subtypes of postsynaptic
neurons that may coexist in discrete regions of the LP, with
each type of postsynaptic neuron receiving afferents from
only one source (however, see Crain and Hall, 1980a). The
possibility that specific dendritic domains of the postsynaptic cell can differentially regulate afferent terminal morphology also remains viable.
Thanks to Jason Glanz for help with the histology and
Chrysty Remillard for photographic assistance. We are
grateful to Dr. Ray Guillery for his helpful comments on an
earlier version of this paper. This work was supported by
NIH grants EY 05504 (S.J.), EY 00126 (G.E.S.), and EY
02621 (vision core grant).
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retina, distinct, posterior, afferents, lateral, terminal, corte, colliculus, thalamic, morphologies, nucleus
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