Download Neurochemical organization of chimpanzee inferior pulvinar complex

THE JOURNAL OF COMPARATIVE NEUROLOGY 484:299 –312 (2005)
Neurochemical Organization of
Chimpanzee Inferior Pulvinar Complex
MONIQUE G. COLA,1–3 BEN SELTZER,2 TODD M. PREUSS,4
1,3
AND CATHERINE G. CUSICK *
1
Department of Structural and Cellular Biology, Tulane University,
New Orleans, Louisiana 70112
2
Department of Psychiatry and Neurology, Tulane University,
New Orleans, Louisiana 70112
3
Department of Neuroscience Training Program, Tulane University,
New Orleans, Louisiana 70112
4
Emory University, Yerkes National Primate Research Center, Atlanta, Georgia 30329
ABSTRACT
The pulvinar of primates, which connects with all visual areas, has been implicated in
visual attention and in control of eye movements. Recently, five separate neurochemical
subdivisions of a region termed the inferior pulvinar complex have been identified in monkeys
(Gray et al. [1999] J Comp Neurol 409:452– 468; Gutierrez et al. [1995] J Comp Neurol
363:545–562), and comparable subdivisions have been mapped in humans (Cola et al. [1999]
NeuroReport 10:3733–3738). In the present study, we investigated the inferior pulvinar of
the chimpanzee (Pan troglodytes), the closest evolutionary relative of humans, using cytochrome oxidase (CO) and acetylcholinesterase (AChE) histochemistry, and immunocytochemistry for calbindin. Each staining method demarcated five histochemical zones corresponding,
from medial to lateral, to the posterior (PIP), medial (PIM), central PIC), lateral (PIL), and the
lateral-shell (PIL-S) divisions in monkeys. The PIP division stained darkly for calbindin and
lightly for CO and AChE. The PIM division was characterized by less neuropil staining for
calbindin, and by distinct, intensely stained patches of CO and AChE. PIC appeared lighter
than adjacent divisions with CO and AChE histochemistry and was moderately stained with
calbindin. PIL was moderately to darkly stained with each method and was adjoined by a
lighter staining shell, PIL-S. Thus, in the aspects of organization we examined, the inferior
pulvinar of chimpanzees closely resembles that of humans and monkeys. This investigation
provides a foundation for more detailed studies of the thalamic relationships of extrastriate
cortex in apes and humans. J. Comp. Neurol. 484:299 –312, 2005. © 2005 Wiley-Liss, Inc.
Indexing terms: visual system; thalamus; primate; evolution
Research in primate neurobiology has traditionally focused on the study of New World and Old World monkeys.
By contrast, there have been relatively few studies of the
ape– human (hominoid) branch of primate evolution,
which separated from the Old World monkey branch ⬃25
million years ago (Fleagle, 1999). Recently, however, there
has been renewed interest in understanding how humans
both differ from and resemble other primates, and this has
fueled new investigations of chimpanzees (Pan troglodytes
and P. paniscus), the great ape species most closely related to humans. New studies have been published comparing humans, apes, and monkeys with respect to neuroanatomy (Preuss et al., 1999; Hackett et al., 2001;
Hopkins and Pilcher, 2001; Semendeferi et al., 2001;
Preuss and Coleman, 2002), gene expression in the brain
© 2005 WILEY-LISS, INC.
(Enard et al., 2002; Cáceres et al., 2003; Clark et al., 2003;
Preuss et al., 2004; Uddin et al., 2004), and cognition
Grant sponsor: National Institutes of Health; Grant number: EY08906
(to C.G.C.); Grant sponsor: APA-MFP Award in Neuroscience (to M.G.C);
Grant sponsor: James S. McDonnell Foundation; Grant number: 98-45;
Grant number: 20002029; Grant number: 21002093 (to T.M.P.).
The last two authors are co-sponsors.
*Correspondence to: Catherine G. Cusick, Department of Structural and
Cellular Biology SL-49, Tulane Medical School, 1430 Tulane Ave., New
Orleans, LA 70112. E-mail: [email protected]
Received 5 August 2004; Revised 16 November 2004; Accepted 22 November 2004
DOI 10.1002/cne.20448
Published online in Wiley InterScience (www.interscience.wiley.com).
300
(Cheney and Seyfarth, 1990; Povinelli and Preuss, 1995;
Povinelli, 2000). These studies make it clear that although
humans share many features of brain organization and
function with apes and monkeys, there are important
differences as well. Documenting the patterns of similarities and difference is essential for understanding how
results derived from nonhuman primates pertain to humans and how evolution modified ancestral primate organization to shape human neural and cognitive specializations.
Like other brain systems, the visual systems of apes and
humans resemble those of nonhuman primates in some
ways, but differ in others (reviewed by Tootell et al., 2003;
Preuss, 2004). For example, humans exhibit features of
primary visual cortex anatomy which have been posited to
represent modifications of the magnocellular (M) pathway
not found in apes or monkeys (Preuss et al., 1999; Preuss
and Coleman, 2002). In addition, there are differences in
the activation patterns of extrastriate and intraparietal
areas between humans and macaque monkeys when subjects view certain classes of moving stimuli, with humans
exhibiting substantial motion-related activity in several
areas that are relatively insensitive to motion in macaques (Orban et al., 2003; Tootell et al., 1997; Vanduffel
et al., 2002). Many aspects of visual system anatomy and
function have not been subjected to detailed comparative
study in primates, however. The anatomy and histochemistry of the pulvinar nucleus of the thalamus has been
extensively studied in New World and Old World monkeys
(Ungerleider et al., 1983; Cusick et al., 1993; Gutierrez et
al., 1995, 2000; Gutierrez and Cusick, 1997; Stepniewska
and Kaas, 1997; Gray et al., 1999; Stepniewska et al.,
1999, 2000; Adams et al., 2000; Soares et al., 2001; Weller
et al., 2002), but has been little studied to date in apes or
humans. Modern studies of the pulvinar in the New World
squirrel monkey and the Old World macaque monkeys
suggest that these animals share a set of homologous
subdivisions of the inferior pulvinar (PI) complex
(Stepniewska and Kaas, 1997; Gray et al., 1999). A recent
study of the human PI complex (Cola et al., 1999), using
histochemical techniques comparable to those used in
monkeys, identified plausible homologs of most of these
divisions, but suggested that one division might be lacking
in humans. In the present study, we used the same histochemical techniques to examine the pulvinar of chimpanzees, and to compare the organization of the chimpanzee
PI to that of humans and monkeys.
The pulvinar nucleus is the largest component of the
subcortical visual system in primates, but its precise functional roles are poorly understood. Because of its extensive
connections with striate and extrastriate cortical visual
areas (for review, see Gutierrez et al., 2000) the pulvinar
is presumed to play an important role in visual processing,
including control of eye movements and directed visual
attention or “visual salience” (Petersen et al., 1985, 1987;
Robinson and Petersen, 1992; Bender and Youakim, 2001;
Karnath et al., 2002), as well as “binding” of perceptual
features (Ward et al., 2002) and semantic-lexical visualauditory functions (Kraut et al., 2003; Crosson, 1999).
Traditionally, the pulvinar has been divided into three
principal nuclei: the medial pulvinar (PM), lateral pulvinar (PL), and inferior pulvinar (PI) (Olszewski, 1952).
This parcellation was based primarily on cytoarchitecture
and the location of prominent fiber bundles, however, and
does not correlate with retinotopic maps (Bender, 1981;
M.G. COLA ET AL.
Ungerleider et al., 1983; Gutierrez and Cusick, 1997).
Recent studies using neurochemical approaches suggest a
pattern of organization more consistent with the topography of connections with different visual areas (Cusick et
al., 1993; Gutierrez and Cusick, 1997; Soares et al., 2001;
Weller et al., 2002; Gray et al., 1999; Stepniewska and
Kaas, 1997; Stepniewska et al., 2000). In Old World and
New World monkeys, the ventral portion of the pulvinar,
consisting of traditional PI and the ventral portion of
traditional PL, constitutes a histochemically distinct area
termed “the inferior pulvinar (PI) complex” (Cusick et al.,
1993; Gutierrez et al., 1995; Gray et al., 1999). The PI
complex in both squirrel and macaque monkeys consists of
five neurochemically distinguishable subdivisions termed
(from medial to lateral): the posterior (PIP), medial (PIM),
central (PIC), lateral (PIL), and lateral-shell (PIL-S) divisions (Gutierrez et al., 1995; Gray et al., 1999; see
Stepniewska and Kaas, 1997, for a slightly different terminology). These histochemical subdivisions, which have
distinctive patterns of connections with known visual areas, cross the dorsal and lateral boundaries of the traditional inferior pulvinar.
The connectional evidence suggests that the neurochemical subdivisions of PI correspond to functionally distinct zones. In monkeys, individual PI subdivisions have
differential connections with visual cortex. For example,
the medial subdivision, PIM, has dense connections with
MT, as well as with DM, suggesting a role for PIM in the
dorsal visual stream and/or in motion processing (Cusick
et al., 1993; Beck and Kaas, 1998; Gray et al., 1999;
Stepniewska et al., 1999, 2000; Adams et al., 2000). PIM
also receives dense inputs from striate cortex, presumably
originating from large motion-sensitive neurons in layer V
(Gutierrez and Cusick, 1997; Rockland, 1998). In contrast
to PIM, the immediately adjacent PIC connects strongly
with the rostral dorsolateral area (DLr) and very little
with area MT (Cusick et al., 1993; Gray et al., 1999; Weller
et al., 2002). The PIC division also receives a dense projection from the superior colliculus that avoids PIM
(Stepniewska et al., 1999, 2000). Compared to monkeys,
the human PI complex was observed to be proportionately
smaller with respect to the pulvinar as a whole, and had
an overall similar staining pattern for AChE, with the
exception that clear evidence for a PIP division was lacking (Cola et al., 1999).
In light of the similarities and differences between
the PI complex in monkeys and humans, the present
study was carried out in chimpanzees to address the
following questions: 1) Can multiple neurochemical subdivisions of the PI complex also be distinguished in
chimpanzees? 2) Are the histochemical staining properties of chimpanzee PI consistent with those seen in
monkeys and humans? 3) Are the subdivisions of PI in
chimpanzees more similar to the pattern in monkeys or
humans? To answer these questions, we examined the
caudal thalamus of chimpanzees with cytochrome oxidase (CO) and acetylcholinesterase (AChE) histochemistry, and immunocytochemical localization of calbindin. Based on number of divisions and fraction of the
pulvinar occupied by the PI complex, our findings indicate that the inferior pulvinar of chimpanzees consists
of a set of neurochemical subdivisions more comparable
to those identified in monkeys than in humans.
CHIMPANZEE INFERIOR PULVINAR
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TABLE 1. Chimpanzee Material Used for This Study1
Case
Hemisphere
Sex
Postmortem Int.
Initial fixative
Later fixative
CH1
R, L
M 28 yr
(est)
20 min (perfused)
perfused with 10% buf.
formalin
CH2
R,L
F 30 yr
5.5 hr
CH3
R, L
F 8 yr (adol)
1 hr
CH4
R, L
F 25 yr (est)
1 hr (perfused)
CH5
R, L
M
1.25 hr (perfused)
4% PFA/.15% glut (4
hr)
10% buf. formalin, 3.5
hr
perfused with saline,
then 2% PFA (5L)
perfused with saline,
4% PFA
CH6
R, L
F
unknown, but prob. ⬇ 1
hr (perfused)
perfused with saline,
4% PFA
CH7
R, L
M
unknown (but ⬍ 12 hrs)
CH8
L
F
unknown (but ⬍ 12 hrs)
10% buf. formalin (6
days)
10% buf. formalin (3
days)
Total
fixation
time
AChE
histochemistry
CO
histochemistry
Calbindin
ICC
10% formalin/
15–25%
sucrose
4% PFA
12⫹ days
(see
note)
2 days
4% PFA
5 days
X
X
X
2% PFA
3 days
X
X
X
4% PFA (1 day)
2% PFA 2
days
4%PFA (2 days)
2% PFA (2
days)
4% PFA 3 days
3 days
X
X
X
4 days
X
X
X
9 days
X
X
X
5 days
X
X
X
4% PFA (1 day)
2% PFA (1
day)
X
X
1
Postmortem interval is the interval between death and the point at which brain was either perfused or removed and placed in fixative.
PFA, buffered paraformaldehyde; Glut., glutaraldehyde; adol., adolescent.
MATERIALS AND METHODS
Chimpanzee thalami (Table 1) were obtained from the
brains of eight adults with no known neurological or behavioral abnormalities housed at the New Iberia Research
Center of the University of Louisiana at Lafayette. These
animals died of natural causes and the postmortem-tofixation intervals ranged from 20 minutes to an unknown
interval that was less than 12 hours. Four brains were
perfused postmortem, one with buffered 10% formalin and
three brains with 2– 4% paraformaldehyde, then blocked
and postfixed for 2 days in buffered formalin plus sucrose,
or buffered 2% paraformaldehyde, respectively. The remaining brains were fixed in buffered 10% formalin for
3.5– 6 days, then blocked and postfixed for 1–3 days in
buffered 4% paraformaldehyde. Hemithalami were dissected from the brain, immersed in 10 –20% buffered sucrose solution at 4°C for 7 days, and then transferred to
cryoprotectant buffer (30% sucrose, 30% ethylene glycol,
1% polyvinylpyrrolidone in 0.1 M phosphate buffer, pH
7.2–7.4; Watson et al., 1986) for 7 days at 4°C. The blocks
were then placed in fresh cryoprotectant buffer and stored
at –20°C. Prior to sectioning, the thalami were transferred
to 40% sucrose in 0.1 M phosphate buffer (pH 7.2–7.4) at
4°C for 5–7 days, then sectioned in the coronal plane at 30
␮m on a freezing microtome. Sections were then stored in
cryoprotectant buffer at –20°C until processed for histochemistry.
Parallel series of sections, at 1:5 to 1:10 intervals, were
processed for chemoarchitecture using an antibody to the
calcium-binding protein, calbindin (monoclonal, 1:4,000,
Sigma, St. Louis, MO; polyclonal, 1:500, Chemicon International, Temecula, CA; Celio, 1990) and standard ABC
methods (Vector kits, Burlingame, CA; Hsu et al., 1981).
Acetylcholinesterase histochemistry was performed following a modification of the Geneser-Jensen and Blackstad (1971) method using acetylthiocholine iodide (Sigma)
as the substrate, followed by development in 1.25% sodium sulfide, and intensification in silver nitrate.
Cytochrome-oxidase histochemistry (Wong-Riley, 1979)
was performed at 37°C on a rotating shaker and intensified by the addition of 0.02 M imidazole buffer (pH 7.6) to
the reaction bath (Preuss et al., 1999).
Sections were viewed under brightfield and darkfield
optics and low-magnification drawings were made by two
independent observers using a camera lucida. Series of
parallel sections were photographed using a Leaf Microlumina digitizing camera. Images were adjusted to produce
sharpness and contrast comparable to gray-scale photographs. Adjacent sections were aligned as semitransparent layers using blood vessels and then corrected for differential shrinkage in Adobe PhotoShop 5.5 (San Jose,
CA). This procedure allowed direct comparison of the locations of candidate subdivisions as visualized with the
different neurochemical methods. Brain sections processed by the same methods available from previous studies of macaque monkeys and humans (e.g., Cola et al.,
1999; Gray et al., 1999) were examined for comparison.
RESULTS
Before presenting findings on the neurochemical organization of the pulvinar of chimpanzees, a brief review of
our previous findings in macaques and humans is presented for comparison. In macaque monkeys, staining of
the PI complex for AChE produced a series of alternating
light and dark bands (Fig. 1), as described previously
(Gutierrez et al., 1995; Cola et al., 1999). A similar alternating dark and light banded pattern was also visualized
with cytochrome oxidase (CO) histochemistry and calbindin immunocytochemistry. The area of densest AChE
stain occurred in PIM, where it formed clusters containing
smaller patches of intense stain (Fig. 1). These patches
appeared to fuse to form a set of curved, vertically oriented
bands. In CO-stained sections (not shown), PIM also displayed patches of intense stain, although not as wide as
were seen with AChE. The posterior (PIP) and central
(PIC) subdivisions, located medially and laterally, respectively, were more lightly stained than PIM by both AChE
and CO histochemistry. The lateral division of the PI
complex, PIL, was moderately stained compared with PIM
and PIC, and adjoined by a lighter shell, PIL-S. In addition,
each staining method revealed divisions that extended
dorsal to the brachium of the superior colliculus (bsc), and
thus outside of the traditional PI nucleus.
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M.G. COLA ET AL.
As previously described (Cola et al., 1999), AChE (Fig.
2) and CO staining (not shown) of the human PI complex
revealed a pattern of alternating dark and light bands
similar to that seen in macaques. A medial region containing small patches of intense stain, comparable to PIM in
macaques, was observed, bordered laterally by an area of
less intense stain (PIC). Lateral to PIC was a zone of more
intense staining (PIL), and lateral to PIL was a band of
lighter AChE and CO stain, similar to PIL-S in macaques.
Using these stains, however, Cola et al. (1999) were not
able to identify in the human PI complex an area comparable to PIP of monkeys.
With regard to chimpanzees, our present observations
suggest an interpretation of inferior pulvinar organization
that departs significantly from previous descriptions in
this species. The differences are shown schematically in
Figure 3, which compares the classical parcellation of the
pulvinar nuclei in chimpanzees with the chemoarchitectonic subdivisions identified in this study. Figure 3A
shows the chimpanzee pulvinar nuclei as described by
Walker (1938) and DeLucchi et al. (1965). Subsequent
neuroanatomical studies of the chimpanzee (Armstrong,
1981; Tigges et al., 1983) have adhered to this parcellation, which was based primarily on cyto- and myeloarchitecture without the benefit of data from connectional studies. The classical PL nucleus of the pulvinar was defined
by the presence of large, mediolaterally oriented fiber
bundles. Rostrally, classical PL was found ventral to the
brachium of the superior colliculus. Further rostrally,
classical PI occupied the entire width of the pulvinar ventral to the bsc and extended ⬃5 mm to the level of the
ventroposterolateral nucleus (VPL). The dorsomedial region of the pulvinar, which lacked distinct fiber bundles,
constituted the medial pulvinar nucleus PM.
In contrast to the earlier parcellation, the present chemoarchitectonic study reveals that the inferior pulvinar in
the chimpanzee encompasses a region that extends more
caudally than the traditional PI and includes the ventral
half of traditional PL and a small, ventral portion of PM as
well. Adhering to nomenclature used for similar regions in
monkeys and humans, we propose the term “PI complex”
for this region.
Just as in the PI complex of monkeys and humans,
separate neurochemical zones were also observed in chimpanzees (Fig. 4). Calbindin (Fig. 4E–H), CO (Fig. 4I–L),
and acetylcholinesterase (Fig. 4M–P) staining demarcated
four histochemical zones corresponding (from medial to
lateral) to the posterior (PIP; e.g., Fig. 4B,F,J,N), medial
(PIM e.g., Fig. 4B,F,J,N), central (PIC e.g., Fig. 4B,F,J,N),
and lateral (PIL e.g., Fig. 4C,G,K,O) divisions in monkeys.
A fifth, lateralmost subdivision (PIL-S) was more readily
distinguishable with calbindin and CO (e.g., Fig. 4G,K).
PIM
At low magnification, the medial region, PIM, had a
distinct patchy appearance in each of the three neuro-
Fig. 1. Low-power photomicrographs of a rostral-to-caudal series
of AChE stained coronal sections, separated by 250 ␮m, through the
PI complex of a macaque monkey. PIP, posterior division of the PI
complex; PIM, medial division; PIC, central division; PIL, lateral division; and PIL-S, lateral-shell. Arrows indicate the dorsal border of PI.
Dorsal is toward the top and lateral is to the right. Scale bar ⫽ 1 mm.
CHIMPANZEE INFERIOR PULVINAR
Fig. 2. A rostral-to-caudal series of sections through human pulvinar complex stained for AChE
histochemistry with camera lucida drawings of PI subdivisions superimposed. Intervals between sections
are 300 ␮m. Modified from Cola et al. (1999). Abbreviations and orientation as in Figure 1. Scale bar ⫽
2 mm.
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304
M.G. COLA ET AL.
the bsc (Fig. 4J,N,I,M). Although the rostrocaudal extent
of PIC was 2.0 –2.5 mm, it did not extend to the rostral pole
of the inferior pulvinar in all cases. In some cases, PIC did
not extend to the rostral pole of the PI complex, but
seemed to wrap around PIM rostrally. In one case at midrostrocaudal levels, PIC and PIP appeared to fuse together
ventrally, suggesting that these seemingly separate divisions might comprise a single zone or “shell” around PIM
(Fig. 5A).
PIL
Fig. 3. Diagrams of the pulvinar complex of the chimpanzee according to (A) the atlas of DeLucchi (1965) and (B) the present study.
The nuclei in A are based on the presence or absence of fiber bundles
in Nissl- or myelin-stained sections. The subdivisions in B are based
on the neuropil and cellular staining patterns for calbindin, AChE,
and cytochrome oxidase. Bsc, brachium of superior colliculus; PulI,
inferior pulvinar nucleus; PulL, lateral pulvinar nucleus; PulM, medial pulvinar nucleus. Other conventions as in Figure 1.
chemical methods used (Fig.4D,H,L,P). At higher magnification, PIM appeared as a conspicuous light zone when
stained for calbindin (Fig. 5A,D), with very light neuropil
stain and sparse calbindin-positive neurons. By contrast,
CO and AChE histochemistry revealed several intensely
stained patches in this zone, resembling the pattern seen
in monkeys and humans. The pattern of densest stain
ranged from patches about 400 ␮m in diameter to elongated bands extending 3.0 mm dorsoventrally (Fig.
4D,H,K,O). This patchiness, as found in monkeys and
humans, suggests a modular organization within PIM.
The PIM subdivision occupied about one-third of the
total area of the classical PI nucleus and was as much as
3.5 mm wide in some individuals. The rostrocaudal extent
ranged from 2.5–3.0 mm. These dimensions notwithstanding, PIM was not confined to classical PI. Approximately
one-third to one-half of PIM extended dorsally across the
brachium of the superior colliculus on individual sections.
Moreover, PIM extended caudal to the bsc, beyond the
caudal limit of traditional PI.
PIP and PIC
The PIP and PIC divisions, which are located, respectively, medial and lateral to PIM, displayed the heaviest
calbindin immunoreactivity for both cells and neuropil
(Fig. 5A–C). By contrast, CO and AChE staining was light
compared to PIM. Adhering to the nomenclature used for
similarly stained and located regions in monkeys and humans, we propose the terms PIP and PIC for these PI
subdivisions.
The posterior subdivision of the PI complex, PIP, is the
smallest, occupying approximately one-fifth the total area
of classical PI. PIP was bordered by PIM laterally and by
the bsc rostrally. Caudally, PIP extended above and then
ended posterior to the bsc. The rostrocaudal extent of PIP
was ⬃1.5 mm.
The central division of the inferior pulvinar, PIC, was
characterized by heavy calbindin staining of neuropil and
cells, and by light AChE and CO stain (e.g., Figs. 4J,N,
5A,C). PIC was a narrow zone located on the lateral border
of PIM, extending rostrally above, and caudally behind,
The PIL subdivision in the chimpanzee was characterized by a band of intense stain demonstrated by all staining methods along the lateral border of PIC. PIL was more
densely stained with CO and AChE, and more darkly
stained for calbindin, than the medially adjacent area PIC
(Fig. 4K,O). Within the lateral compartment of this zone,
there was a dense population of small calbindin-stained
neurons interspersed with a small number of large, darkly
stained neurons (Fig. 5E). The small calbindin-stained
neurons had moderately stained somas with a few lightly
stained dendrites, whereas larger immunoreactive neurons had a darkly stained soma with dark radiating dendrites. While the calbindin immunoreactivity appeared
homogenous in PIL, AChE and CO histochemistry revealed areas of slight patchiness or heterogeneity (Fig.
4J,N).
PIL corresponded to the entire rostral and approximately one-third of the caudal extent of classical PI, measuring ⬃3.0 mm in the rostrocaudal dimension. PIL also
extended dorsal to the bsc, into traditional PL, and ended
caudal to the bsc (Fig. 4I,M).
PIL-S
PIL was adjoined laterally by a narrow “shell” zone of
lighter staining by all three methods. The intensely
stained calbindin “giant” cells described in squirrel monkeys and macaques (Cusick et al., 1993; Gray et al., 1999)
were also visible in this region (Figs. 6, 7). PIL-S extended
dorsally into traditional PL, and scattered large calbindin
cells were found in PL and PM. PIL-S was typically visible
for ⬃1.5 mm from rostral to caudal with a width of ⬃1.0 –
2.0 mm. Just as for the other divisions, it extended above
and caudal to the bsc.
DISCUSSION
The present investigation shows many qualitative similarities between the neurochemical organization of the PI
complex of chimpanzees and that of New World monkeys,
Old World monkeys, and humans. Table 2 summarizes the
staining characteristics of each PI subdivision in chimpanzees for each of the neurochemical markers employed.
Similar staining patterns within the PI complex across
species have now been demonstrated using AChE, CO,
and calbindin (Cusick et al., 1993; Gutierrez et al., 1995;
Stepniewska and Kaas, 1997; Cola et al., 1999; Gray et al.,
1999). As five distinct but comparable subdivisions were
identified in the chimpanzee, we propose to apply the
same nomenclature to this species as was used for macaques and humans (Cola et al., 1999; Gray et al., 1999).
The AChE, CO, and calbindin stains reliably revealed the
boundaries of four subdivisions (PIP, PIM, PIC, and PIL) in
the chimpanzee PI complex. Cytochrome oxidase histochemistry and calbindin immunocytochemistry demar-
CHIMPANZEE INFERIOR PULVINAR
cated the boundary between PIL and PIL-S more consistently than did AChE.
Although we did not undertake quantitative morphometric comparisons, there appeared to be differences between species in the proportions of different divisions of
the pulvinar. In humans, we could identify no counterpart
of the PIP division we have identified in chimpanzees and
in monkeys. For reasons discussed below, we consider PIP
to likely be an extension of PIC, rather than a distinct
division of PI in its own right. Under this interpretation,
the lack of a PIP in humans would represent the morphological reduction of PIC–PIP rather than the loss of a
discrete subnucleus. Nevertheless, the existence of a clear
PIP division in chimpanzee is more similar to monkeys
than to human. It is also noteworthy that the histochemical border of the PI complex, within the pulvinar as a
whole, was in a proportionately more dorsal location in
both monkeys and chimpanzees compared to humans.
This suggests that the PI complex, interconnected with
early visual areas, is larger, relative to PM and dorsal PL,
in chimpanzees than in humans. The pulvinar, considered
as a whole, is much larger in humans than in chimpanzees
or other great apes (Armstrong, 1981), and it seems likely
that the PM, which projects to many regions of higherorder association cortex, underwent a greater degree of
expansion in human evolution than did the PI complex,
which projects mainly to striate and extrastriate visual
cortex (see Gutierrez et al., 2000, for review).
These differences in adult pulvinar structure in different primate lines may be linked to observations that the
human pulvinar contains cell populations that are not
found in macaques or in nonprimate mammals. Earlier
histological observations indicated a telencephalic origin
for some of the neurons in the human pulvinar (Rakic and
Sidman, 1969; Sidman and Rakic, 1973). Building on
those studies, Letinic and Rakic (2001) showed that a
population of GABAergic neurons in human thalamus
originates from the ganglionic eminence of the telencephalon. It may be that the evolutionary enlargement of the
human thalamus, in particular the association nuclei, and
especially the pulvinar, resulted from a developmental
influx of neurons from the telencephalon via a migratory
stream not found in other mammals (Letinic and Kostovic,
1997). Such neurons are not found in monkeys or rodents,
but the status of chimpanzees in this regard has not yet
been investigated. The contribution of the ganglionic eminence to the thalamus could be a human specialization, or
it could be an ape-human specialization.
The distribution of calbindin-positive neurons and neuropil staining within the chimpanzee PI complex resembled that of macaque monkeys. As in other species, the
PIM, the “calbindin hole” (Cusick et al., 1993) of neurochemically defined PI, contained light neuropil staining
and sparse calbindin-stained neurons. This feature, together with the dense staining for CO, suggests that, like
monkeys and humans, the chimpanzee PIM has neurochemical features resembling those of primary sensory
relay nuclei of the thalamus (Cusick et al., 1993) such as
the ventroposterior and medial geniculate nuclei (Hashikawa et al., 1991; Rausell and Jones, 1991; Rausell et al.,
1992a,b). In all of these structures, compartments or layers that are dense in CO are also poor in calbindin. This
staining pattern also characterizes thalamic compartments with fast sensory conduction and secure transmission and has been termed “lemniscal” (Cusick et al., 1993).
305
Interestingly, the driving afferents to PIM and from there
to the motion processing area MT appear to originate from
large layer V neurons in the striate cortex (Gutierrez and
Cusick, 1997; Rockland, 1998; Feig and Harting, 1998).
The patchy staining of PIM with AChE and CO found in
chimpanzees agrees well with the pattern of intense and
lighter stain described previously in Old World and New
World monkeys (Lin and Kaas, 1979; Stepniewska and
Kaas, 1997; Cusick et al., 1993; Gutierrez et al., 1995;
Gutierrez and Cusick, 1997; Gray et al., 1999) and in
humans (Cola et al., 1999). The consistent presence of
patches in different species suggests modularity within
PIM. Connectional studies in macaque and squirrel monkeys (Cusick et al., 1993; Gutierrez et al., 1995; Gutierrez
and Cusick, 1997; Gray et al., 1999; Adams et al., 2000;
Stepniewska et al., 1999) have shown reciprocal connections between PIM and cortical area MT. Other connectional studies involving injections of tracers into area V1
or MT have also revealed patches of connections in PIM
(Gutierrez and Cusick, 1997; Gray et al., 1999). Thus,
these separate patches of stain in PIM may reflect discrete
connectional units within this subdivision.
The zones immediately adjacent to PIM (PIP and PIC)
displayed dense calbindin immunoreactivity, with many
darkly stained neurons and heavy staining of the neuropil. In one case immunostained for calbindin, PIP and PIC
appeared to fuse ventrally, suggesting that they may actually be a single division. In macaque and squirrel monkeys, both PIP and PIC interconnect with rostral dorsolateral cortex, DLr (Cusick et al., 1993; Steele and Weller,
1993; Gray et al., 1999), and receive input from the superficial layers of the superior colliculus (Stepniewska et al.,
1999, 2000), again supporting the possibility that these
two zones are a single division. In light of this possibility,
the apparent absence of a PIP division in humans (Cola et
al., 1999) may not represent a true difference in numbers
of subdivisions, but rather a limited medial extent of a
“shell” zone with respect to PIM.
The largest PI subdivision, PIL, as identified by calbindin,
was densely stained and characterized by containing large
darkly stained neurons within a population of smaller lightly
stained neurons. Rostrally, PIL occupied the full mediolateral width of the inferior pulvinar, while caudally it extended
to the caudal pole. PIL-S, the laterally adjoining subdivision,
had lightly stained neuropil with calbindin, but contained
numerous giant calbindin cells. PIL-S is more clearly distinguishable as a zone separate from PIL with calbindin and CO
than with AChE. Connections of V1, MT, and the DL region
in monkeys separately target PIL-S in a retinotopically organized fashion and support its existence as a distinct division
from PIL (Cusick et al., 1993; Gutierrez and Cusick, 1997;
Gray et al., 1999).
There are few existing studies of the subcortical connections of the pulvinar in chimpanzees. Walker (1939) reported that, following ablation of the occipital lobe posterior to the parieto-occipital fissure, and the posterior
temporal region, retrograde degeneration occupied the
traditional PL and PI. The degeneration continued rostrally in the same relative position to the anterior pole of
the PI nucleus. While these results were obtained without
the benefit of neurochemically defined pulvinar subdivisions or modern tracing methods, the regions of degeneration would appear to correspond to the PI complex.
Injections of horseradish peroxidase into cortical areas
17 and 18 in chimpanzee brains labeled cells in the tradi-
306
Fig. 4. Line drawings of chimpanzee PI subdivisions (A–D) and
low power darkfield images of calbindin stained sections from the
same levels (E–H). Note the staining patterns of individual subdivisions consistently rise above the bsc. I–L: PI complex shown with
M.G. COLA ET AL.
cytochrome oxidase and with AChE stains (M–P). Rostral-to-caudal
series: The within-series spacing (e.g., A–B, B–C, C–D) is 300 ␮m and
the between-series spacing (e.g., A–E, B–F) is 60 ␮m. Arrows indicate
dorsal border of PI. Conventions as in Figure 2. Scale bars ⫽ 1 mm.
CHIMPANZEE INFERIOR PULVINAR
307
Figure 4
tional inferior and lateral pulvinar (Tigges et al., 1983).
The resulting cluster of label in the inferior pulvinar was
situated ventral to the bsc at the level of the posterior
(Continued)
LGN and was confined to the area between the lateral and
medial geniculate nuclei. The labeled neurons stretched
rostrocaudally for ⬃1.5 mm and formed longitudinal
Fig. 5. Distribution of calbindin-positive neurons and neuropil staining within neurochemically
delineated PI subdivisions. Each region indicated in (A) is shown at higher magnification in the lower
panels (B–E). Conventions as in Figure 3. Scale bar ⫽ 500 ␮m in A; 90 ␮m in D (applies to B–E).
CHIMPANZEE INFERIOR PULVINAR
309
Fig. 6. Calbindin immunostaining in PIL and PIL-S. Densely stained calbindin positive cells are found
medially, while the most lateral region PIL-S contains numerous darkly stained neurons embedded in a
more lightly stained neuropil. Dashed line mark the boundary between PIL to the left and PIL-S to the
right. Dorsal is toward the top. LGN, lateral geniculate nucleus. Scale bar ⫽ 0.5 mm.
bands that extended beyond the classically defined boundaries of the inferior pulvinar. These results are in agreement with similar connectional studies in macaque monkeys (Gutierrez and Cusick, 1997). While connectional
data in chimpanzees are limited (Walker, 1939; Tigges et
al., 1983), the observation that connections do not conform
to classical boundaries of the pulvinar is consistent with
data from other species (Gray et al., 1999) and supports
the present data regarding neurochemical subdivisions of
the inferior pulvinar.
The present study correlated three different neurochemical methods on neighboring serial sections to define
the location and internal organization of the chimpanzee
inferior pulvinar complex. Separate neurochemical subdivisions within the chimpanzee PI suggest functional differences reflected by their patterns of cortical connections.
In monkeys, individual subdivisions connect with several
visual areas and individual visual areas connect with several subdivisions (e.g., Gutierrez and Cusick, 1997; Gray
et al., 1999; Adams et al., 2000). Homologous subdivisions
in chimpanzee may have similar characteristics. If the
chimpanzee PI complex corresponds, as in monkeys, to the
portion of pulvinar connected to retinotopically organized
visual areas V1, V2, V4 (Cusick et al., 1993; Gutierrez and
Cusick, 1997; Robinson and Cowie, 1997), then the PI
complex might be involved in processing color, form, and
motion of a visual stimulus. The dense connections of area
MT in monkeys to PIM (Cusick et al., 1993) suggest a role
for this division in motion processing in chimpanzees as
well.
Taking a broader, evolutionary perspective, the present
comparative data suggest that the PI complex is a primate
trait that co-evolved with motion processing areas of the
superior temporal region. In all primates that have been
examined with calbindin immunocytochemistry, there is a
medial oval of decreased stain within the classical inferior
pulvinar. This “calbindin hole” is flanked by areas of
denser stain which laterally become alternating bands of
medium and darker stain (Cusick et al., 1993; Gutierrez et
al., 1995; Beck and Kaas, 1998; Adams et al., 2000; Soares
et al., 2001; present study). Similarly, in the posterior
superior temporal cortex, primates exhibit a densely myelinated motion processing area MT which is surrounded
by a more lightly myelinated rim of cortex (Cusick et al.,
1984; Desimone and Ungerleider, 1986). MT is connected
with the “calbindin hole” while the myelin-light rim of MT
is connected with the calbindin dark rim of PIM (Cusick et
al., 1993; Gray et al., 1999; Weller et al., 2002). These
striking patterns of thalamic histochemistry and functional connectivity are absent in common laboratory ani-
310
M.G. COLA ET AL.
Fig. 7. Low-power view in PIL-S showing representative calbindin “giant” cells with radiating dendrites as well as numerous smaller calbindin cells. Scale bar ⫽ 100 ␮m.
TABLE 2. Neurochemical Characteristics of Chimpanzee PI Complex
Subdivisions
Cytochrome
oxidase
AChE
Calbindin
PIP
PIM
PIC
PIL
PIL-S
light
intense/patchy
light
dark
moderate
light
intense/patchy
light
dark
moderate
moderate
very light
moderate
dark
moderate, with large
darkly stained cells
mals such as rats and the domestic cat. This further
suggests a restricted evolutionary history of the inferior
pulvinar complex and superior temporal lobe visual areas
to the primate line.
ACKNOWLEDGMENT
We thank the staff of the New Iberia Research Center
for assistance in obtaining chimpanzee tissue.
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