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Histological definition of the vomeronasal organ in humans and chimpanzees with a comparison to other primates.

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THE ANATOMICAL RECORD 267:166 –176 (2002)
Histological Definition of the
Vomeronasal Organ in Humans and
Chimpanzees, With a Comparison to
Other Primates
TIMOTHY D. SMITH,1,2* KUNWAR P. BHATNAGAR,3 KRISTIN L. SHIMP,1
JONATHAN H. KINZINGER,1 CHRISTOPHER J. BONAR,4
ANNIE M. BURROWS,2,5 MARK P. MOONEY,2,6 AND MICHAEL I. SIEGEL2
1
School of Physical Therapy, Slippery Rock University, Slippery Rock, Pennsylvania
2
Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania
3
Department of Anatomical Sciences and Neurobiology, University of Louisville
School of Medicine, Louisville, Kentucky
4
Cleveland Metroparks Zoo, Cleveland, Ohio
5
Department of Physical Therapy, Duquesne University, Pittsburgh, Pennsylvania
6
Department of Oral Medicine and Pathology, University of Pittsburgh,
Pittsburgh, Pennsylvania
ABSTRACT
The vomeronasal organ (VNO) is a chemosensory structure that has morphological indications of functionality in
strepsirhine and New World primates examined to date. In these species, it is thought to mediate certain socio-sexual
behaviors. The functionality and even existence of the VNO in Old World primates has been debated. Most modern texts
state that the VNO is absent in Old World monkeys, apes, and humans. A recent study on the VNO in the chimpanzee (Smith
et al., 2001b) challenged this notion, demonstrating the need for further comparative studies of primates. In particular, there
is a need to establish how the human/chimpanzee VNO differs from that of other primates and even nonhomologous mucosal
ducts. Histochemical and microscopic morphological characteristics of the VNO and nasopalatine duct (NPD) were examined
in 51 peri- and postnatal primates, including humans, chimpanzees, five species of New World monkeys, and seven
strepsirhine species. The nasal septum was removed from each primate and histologically processed for coronal sectioning.
Selected anteroposterior intervals of the VNO were variously stained with alcian blue (AB)-periodic acid-Schiff (PAS), PAS
only, Gomori trichrome, or hematoxylin-eosin procedures. All strepsirhine species had well developed VNOs, with a
prominent neuroepithelium and vomeronasal cartilages that nearly surrounded the VNO. New World monkeys had variable
amounts of neuroepithelia, whereas Pan troglodytes and Homo sapiens had no recognizable neuroepithelium or vomeronasal
nerves (VNNs). Certain unidentified cell types of the human/chimpanzee VNO require further examination (immunohistochemical and electron microscopic). The VNOs of P. troglodytes, H. sapiens, and New World monkeys exhibited different
histochemistry of mucins compared to strepsirhine species. The nasopalatine region showed great variation among species.
It is a blind-ended pit in P. troglodytes, a glandular recess in H. sapiens, a mucous-producing duct in Otolemur crassicaudatus, and a stratified squamous passageway in all other species. This study also revealed remarkable morphological/
histochemical variability in the VNO and nasopalatine regions among the primate species examined. The VNOs of humans
and chimpanzees had some structural similarities to nonhomologous ciliated gland ducts seen in other primates. However,
certain distinctions from the VNOs of other primates or nonhomologous epithelial structures characterize the human/
chimpanzee VNO: 1) bilateral epithelial tubes; 2) a superiorly displaced position in the same plane as the paraseptal
cartilages; 3) a homogeneous, pseudostratified columnar morphology with ciliated regions; and 4) mucous-producing structures in the epithelium itself. Anat Rec 267:166 –176, 2002. © 2002 Wiley-Liss, Inc.
Key words: vomeronasal complex; histochemistry; mucous glands; mucins; VNO
Grant sponsor: College of Health and Human Services, Slippery Rock University; President’s Academic Initiatives, Slippery
Rock University.
*Correspondence to: Dr. Timothy D. Smith, School of Physical
Therapy, Slippery Rock University, Slippery Rock, PA 16057.
Fax: (724) 738-2113. E-mail: timothy.smith@sru.edu
©
2002 WILEY-LISS, INC.
Received 6 June 2001; Accepted 5 March 2002
DOI 10.1002/ar.10095
Published online 00 Month 2002 in Wiley InterScience
(www.interscience.wiley.com).
167
PRIMATE VOMERONASAL ORGAN AND NASOPALATINE DUCT
TABLE 1. Age group, preservation, and source of the primate species investigated species*
Mirza coquereli (Coquerel’s dwarf lemur)
Microcebus murinus (Grey lesser mouse lemur)
Eulemur mongoz (Mongoose lemur)
Galago moholi (Mohol’s galago)
Galagoides demidoff (Dwarf galago)
Otolemur crassicaudatus (Fat-tailed bushbaby)
O. garnettii (Garnett’s bushbaby)
Callithrix jacchus (White ear-tufted marmoset)
Leontopithecus rosalia (Golden lion tamarin)
L. chrysomelas (Golden-headed lion tamarin)
Saguinus geoffroyi (Geoffroy’s tamarin)
Alouatta caraya (Black howler monkey)
Homo sapiens (Human)
Pan troglodytes (Common chimpanzee)
n
Agea
Preservationb
Sourcec
1
2
1
1
1
4
4
2
3
1
6
1
21
3
1
3
1
1
1
3
3
3
1, 2
3
1, 2, 3
3
2, 3
2, 3
a
a
b
a
a
b
b
b
b
b
b
a
c, d
a, b
DUPC
DUPC
CMZ
DUPC
DUPC
DUMC
DUMC
DUMC
CMZ
CMZ
CMZ
CMZ
SRU
UP, CMZ
*Classification according to Nowak (1999).
1, neonate; 2, infant/juvenile; 3, adult.
b
a, frozen, later immersed in formalin; b, immersed in formalin after death; c, embalmed; d, immersed in Bouin’s solution.
c
CMZ, Cleveland Metroparks Zoo; DUMC, Duke University Medical Center; DUPC, Duke University Primate Center; SRU,
Slippery Rock University; UP, University of Pittsburgh.
a
For more than a century, it has been thought that humans possess at least a postnatal remnant of the vomeronasal organ (VNO) (Kölliker, 1877; Potiquet, 1891),
whereas other Old World primates lack any trace of the
VNO postnatally (Loo, 1973; Zingeser, 1984; Ankel-Simons, 2000). This has led to confusion regarding the homology of the human VNO to that of other mammals (see
Smith et al., 2001a). Recent work has shown that chimpanzees also possess a VNO during postnatal ontogeny
(Smith et al., 2001b), which partly resolves this issue. At
the same time, such findings hint that the degree of variability of the VNO among primates may be greater than
previously thought. In a recent review, Smith et al.
(2001a) sought to define character states to account for the
variation. However, delineating the unique characteristics
of the human or chimpanzee VNO has remained difficult.
Humans and chimpanzees have VNOs that are more
superiorly positioned compared to those of other primates
(Smith et al., 2001b). This atypical location, combined
with a markedly different (simplified) epithelial morphology creates a difficulty in that such a structure may be
easily confused with other mucosal structures, such as
gland ducts or remnants of the nasopalatine duct (NPD)
(see Jacob et al., 2000; Bhatnagar and Smith, 2001; Smith
et al., 2001c). It is therefore essential to morphologically
define the “VNO character state” of chimpanzees and humans. Such a clarification will augment a reexamination
of other catarrhine primates for VNO presence or absence,
and will ultimately lead to a better understanding of the
evolution of this chemosensory system among the Haplorhini (Old World monkeys, New World monkeys, tarsiers,
apes, and humans).
Among all haplorhine primates, the human VNO has
received the most attention to date. The function of the
human VNO is highly debated (Grosser et al., 2000;
Wysocki and Preti, 2000; Bhatnagar and Smith, 2001;
Kouros-Mehr et al., 2001), in part due to the scarcity of
comparative studies to place the structure in proper context (Smith et al., 2001a). Certain histochemical and morphological aspects of the human VNO differ markedly
from those of other mammals (Roslinski et al., 2000; Bhatnagar and Smith, 2001). Mucin produced in the human
VNO appears histochemically similar to that of respira-
tory epithelium (acidic and neutral mucin production),
and the VNO appears to act both in secretion (via goblet
cells and other intraepithelial glands) and transport
(Roslinski et al., 2000; Bhatnagar and Smith, 2001). In
contrast, the vomeronasal glands of most other mammals
are more elaborate and produce mucins that differ histochemically (primarily neutral mucins) from other glands
of the nasal cavity (Roslinski et al., 2000). Few studies
have compared the histochemistry of the VNO among
primates (Hunter et al., 1984), and the histochemical
characteristics of the VNO in chimpanzees are still poorly
understood. It is also unclear how the VNO and remnants
of the NPD in humans and chimpanzees compare to those
of other primate species or to other duct-like structures
within the nasal mucosa. The present study examines the
vomeronasal and NPD regions of the nasal septum among
primates in order to provide a clearer morphological/histochemical definition of the VNO in humans and chimpanzees.
MATERIALS AND METHODS
Cadaveric nasal septal tissues from 51 primates (adults
except as noted; see Table 1), including Pan troglodytes
(two juveniles, one adult), Homo sapiens (one juvenile, 20
adults), Saguinus geoffroyi (three neonates, two juveniles,
one adult), Leontopithecus rosalia (two neonates, one juvenile), Leontopithecus chrysomelas, Callithrix jacchus,
Alouatta caraya, Mirza coquereli (one neonate), Microcebus murinus, Eulemur mongoz (one neonate), Galago moholi (one neonate), Galagoides demidoff (one neonate),
Otolemur garnettii, and O. crassicaudatus were examined.
Tissues were obtained from gross anatomy laboratories,
research laboratories, Duke University Primate Center,
and the Cleveland Metroparks Zoo. Initial methods of
preservation involved freezing, embalming, or immersion
in 10% buffered formalin (Table 1), but all specimens were
stored for at least 2 days in 10% buffered formalin prior to
decalcification and histological processing. Either the entire head or one-half of the head was processed in the
perinatal primates. In all other cases, resected septa were
used. Tissues were decalcified in a formic acid solution
(formic acid-sodium citrate or Cal-Ex II; Fisher Scientific,
Pittsburgh, PA), dehydrated in an ethanol series, cleared
168
SMITH ET AL.
Figure 1.
169
PRIMATE VOMERONASAL ORGAN AND NASOPALATINE DUCT
TABLE 2. Morphological and histochemical observations on the primate species investigated
Epithelial morphology
Species
Mirza coquereli
Microcebus murinus
Eulemur mongoz
Galago moholi
Galagoides demidoff
Otolemur crassicaudatus
Otolemur garnettii
Callithrix jacchus
Leontopithecus rosalia
L. chrysomelas
Saguinus geoffroyi
Alouatta caraya
Homo sapiens
Pan troglodytes
NPD
VNO
NP
VND
VNO
AB
PAS
AB
PAS
StSq
StSq
StSq
StSq
StSq
StSq
StSq
StSq
StSq
NA
StSq
StSq
PSt,C
StSq,PSt,C
StC
StC
StC
StC
StC
StSq, K
StSq, K
StSq
St-Sq/StC
NA
StC
StC
StC
StC
StC, NE
SiC, NE
StC, NE
StC, NE
SiC/StC, NE
StC/PSt, NE
StC/PSt, NE
PSt, NE
SiC/StC/PSt, NE
SiC/StC/PSt, NE
SiC/StC/PSt, NE
StC/PSt, NE?
PSt,C
PSt,C
–
–
–
–
–
⫹⫹
–
–
–
NA
–
–
⫹⫹
⫹⫹
–
–
–
–
–
⫹⫹
–
–
–
NA
–
–
⫹⫹
⫹⫹
–
–
–
–
–
⫹⫹a
–
⫹⫹
⫹
⫹
⫹
⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹⫹
⫹
⫹
⫹
⫹
⫹⫹
⫹⫹
a
AB⫹ seen only in region of the VNO duct.
NP, nasopalatine duct region (duct or remnant); VND, vomeronasal organ duct; VNO, vomeronasal organ; AB, alcian blue;
PAS, periodic acid-Schiff; C, ciliated; K, keratinized cells at apex; NE, neuroepithelium; PSt, pseudostratified, columnar; SiC,
simple cuboidal/columnar; StC, stratified cuboidal/columnar; StSq, stratified squamous; ⫹, restricted patches of tissue with
AB/PAS positivity; ⫹⫹, widespread AB/PAS positivity seen; –, no AB/PAS positivity seen; NA, relevant tissue not available.
in xylene, embedded in paraffin, and serially sectioned in
the coronal plane at 10 –25 ␮m. Every 10th section was
mounted on glass slides and alternately stained with hematoxylin-eosin and Gomori trichrome protocols. The tissues were examined for the presence of the VNO using a
Leica photomicroscope. In each specimen, both the nasopalatine and more posterior regions were examined for
structures resembling either the human/chimpanzee VNO
(Johnson et al., 1985; Smith et al., 2001a) or the generalized mammalian VNO (Ciges et al., 1977; Breipohl et al.,
1979). The beginning and end points of the VNO were
identified, and the 1st, 25th, 50th, 75th, and 100th percentiles of the VNO length were noted. Unstained sections
that approximated each anteroposterior (or rostrocaudal)
percentile were mounted on glass slides and stained with
a combined alcian blue (AB)-periodic acid-Schiff (PAS)
protocol to ascertain the presence of acidic (AB⫹) or neutral (PAS⫹) mucins (Humason, 1979). Selected sections
from each species were also mounted on glass slides and
stained with PAS only, to verify whether AB may have
masked the affinity of PAS⫹ structures.
Each series was examined at ⫻25 to ⫻1,000 by light
microscopy to describe the histological structure of the
VNOs and other mucosal structures. Numerous aspects of
the primate VNOs in the present study were compared to
those of humans as previously described (Roslinski et al.,
2000; Bhatnagar and Smith, 2001). In addition, the apex
of the VNO epithelium was carefully examined using human and chimpanzee specimens, and cilia were clearly
seen in all sections. Cilia were examined with regard to
circumferential distribution (i.e., to what extent they lined
the apex of the VNO epithelium in coronal cross-section)
and with regard to anteroposterior distribution (i.e.,
whether they were seen at a particular anteroposterior
level). Associated glandular tissues were described by examining sections stained with an AB/PAS protocol. Characteristics of the tissues were then compared among species at similar anatomical levels. To control for the
possibility that PAS⫹ structures contained glycogen and
not mucins, a series of sections containing the VNO were
soaked in diastase of malt solution at 37° for 1 hr (Humason, 1979). The slides were then stained with another
control series of adjacent sections in PAS.
Fig. 1. A: Coronal section showing the vomeronasal duct (open
arrow) and (slightly posteriorly on the other side) the VNO in a neonatal
Galago moholi. The section is posterior to the connection of the vomeronasal duct and the nasopalatine duct (NPD). B: Coronal section of the
VNO in Mirza coquereli (neonate) showing the precocious development
of the organ. Note the thicker, medial sensory epithelium. C: The VNO of
an adult Otolemur crassicaudatus, showing the thicker, medioventral
neuroepithelium (VNNE) and thinner, lateral nonsensory epithelium (NSE)
and adjacent VNNs. D: The NSE of an adult Otolemur crassicaudatus.
Note the nonciliated, simple columnar epithelium. E: The VNNE of an
adult Otolemur crassicaudatus. Note the dense population of receptor
cells (white arrows) and microvillar apex (small open arrows). F: Coronal
section showing the VNOs of a 1-month-old Saguinus geoffroyi. G: Note
that in the magnified view sparse receptor cells (white arrows) can be
seen in the VNO epithelium. H: The VNO of an adult Callithrix jacchus
exhibited a uniform sensory epithelium (white arrows indicate receptor
nuclear layer) at nearly all anteroposterior levels. I: Posteriorly, the VNO
of L. rosalia (4-month-old shown) resembled that of strepsirhines (small
arrows indicate medioventral neuroepithelium). J: The VNO of a juvenile
chimpanzee shows the typical enlarged lumen (L ⫽ lumen) and abundant
communicating glands (GD ⫽ gland duct). K: The region of the gland
duct is enlarged to show certain nonciliated, unidentified cells with round
nuclei (small arrows). NS ⫽ nasal septum; VNC ⫽ vomeronasal cartilage.
Scale bars: A ⫽ 300 ␮m; B, I, J ⫽ 150 ␮m; C ⫽ 150 ␮m; D, E, H, and K ⫽
40 ␮m; F ⫽ 600 ␮m; G ⫽ 30 ␮m.
RESULTS
VNOs were found in all primates, although with variable morphology (Fig. 1). In several specimens, epithelial
damage (interpreted as freezing artifacts that occurred in
two of the specimens that were frozen before fixation)
prevented certain morphological observations, as noted
below. VNOs of all strepsirhine species exhibited a well
defined vomeronasal neuroepithelium (VNNE ) at all ages
170
SMITH ET AL.
Figure 2.
PRIMATE VOMERONASAL ORGAN AND NASOPALATINE DUCT
171
(Fig. 1A–D) and nonsensory epithelium (NSE) (Fig. 1E;
Table 2). The VNO epithelia of New World species were
more highly variable. A clear VNNE was found in small
patches in neonatal S. geoffroyi and Leontopithecus spp.,
but was more widely distributed in juveniles and adults
(Fig. 1F, G, and I). In both genera, VNNE could be found
on all sides of the VNO (superior, inferior, medial, and
lateral) and was sometimes interrupted by segments of
NSE. Callithrix jacchus was characterized by a homogeneous sensory lining in the VNO (Fig. 1H), with only
minute portions of NSE. In all callitrichids, receptor populations appeared to be more dense toward the posterior
half of the VNO. Neonatal and juvenile L. rosalia showed
a remarkable morphology in the posterior one-fourth of
the VNO, in which the organ resembled that of strepsirhines, with a medial VNNE and a lateral NSE (Fig. 1I).
The VNO epithelium of A. caraya was difficult to interpret
due to apparent damage from freezing (disrupted epithelia), but some small segments of stratified or pseudostratified NSE could be seen. In addition, VNNs superior to the
VNO (and ascending in an anteroposterior direction from
the VNO) suggested the likely existence of a VNNE in
disrupted regions.
The NSE of the VNO in all strepsirhines and New World
monkeys was generally nonciliated epithelium of variable
morphology (Fig. 1D; Table 2), but isolated ciliated cells
were sometimes seen—for example, in the more posterior
portions of NSE in Otolemur spp. Vomeronasal ducts were
lined with stratified cuboidal epithelia in all strepsirhine
and New World monkeys, but had some apparent keratinization in some species (Table 2). In addition, the vomeronasal duct of O. crassicaudatus had intraepithelial mucous glands in the duct wall.
The VNOs of P. troglodytes and H. sapiens were more
simplified oval or round tubes (Figs. 1J, and 2A and F).
Initially, these were lined with stratified cuboidal epithelia, and made a transition to pseudostratified, columnar
epithelia within 50 –100 ␮m. In most specimens, the
pseudostratified columnar epithelia were nonciliated for
the first several (anterior) sections, and later sections
contained cilia projecting into the lumen from all sides,
with small gaps of nonciliated cells (Fig. 2D and E). As
reported previously (Smith et al., 1998), some human
VNOs were not suitable for identifying cilia due to distortion or apparent tissue decay that obscured the epithelial
apex of the VNO. Using more recently sectioned material
(Smith et al., 2001c), three human septa were suitable for
serial anteroposterior examination for distribution of cilia.
All chimpanzees had at least some discernable cilia, but
only one had sufficient preservation to reveal that cilia
were present in all anteroposterior sectional levels (Fig.
2B–E). The anteroposterior distribution of cilia varied
among humans. In the 2-year-old human, the anterior
two-thirds of the VNO was nonciliated. In most of the
posterior one-third, the apex of the VNO epithelium was
almost completely ciliated, with small patches of nonciliated cells. A 77-year-old male human exhibited nearly
continuous cilia (circumferentially) in the VNO for most of
the length following the short, stratified cuboidal “duct”
(Fig. 2G), although the posterior-most sections had no cilia
(Fig. 2I). A 79-year-old male exhibited variation in the
circumferential distribution of cilia, from nearly continuous to patchy. Both of these adults displayed markedly
different distributions of cilia on the right and left VNOs,
with one side having a more continuous circumferential
presence of cilia.
In both P. troglodytes and H. sapiens, the presence of
dark lines suggestive of basal bodies were also seen at the
apex of ciliated cells (Fig. 2D and G). Basal cells could also
be seen, and gaps in the line of basal bodies (Fig. 2D) were
seen where goblet cells or at least one other type of columnar cell intervened among ciliated cells. The latter cells
were more rare than other types, were nonciliated, and
had nuclei within the middle region of the VNO. In one
juvenile P. troglodytes, certain of these cells had round,
dark nuclei and were sparsely scattered throughout the
epithelium (Fig. 1J–K). There were no apparent unmyelinated nerves in the adjacent lamina propria.
There were some structures resembling the VNOs of
humans and chimpanzees in the other primates—specifically unilateral, ciliated gland ducts. In general, most
gland ducts were lined with simple cuboidal epithelia and
were nonciliated, but in one strepsirhine (E. mongoz) a
unilateral epithelial duct that bore some resemblance to
the human/chimpanzee VNO was seen. This duct ended
70 ␮m anterior to the sectional level of the NPD and thus
had no direct connection to the VNO. It was found in the
same sectional plane and was spatially separated from the
lamina transversalis anterior. The duct was clearly ciliated and had associated AB–/PAS– glandular tissue. The
left VNO of one L. rosalia neonate also ended in a ciliated
gland duct; cilia were observed in gland ducts entering the
superior pole of the VNO in C. jacchus.
In all strepsirhines and New World primates, the NPD
was lined with stratified (usually squamous) epithelium
(Fig. 3; Table 2). In P. troglodytes, a partially patent NPD
was seen, completely fused on the oral (anteroinferior)
aspect (Figs. 3E and 4J). It was mainly lined with stratified squamous epithelium, although large patches of respiratory (pseudostratified columnar) epithelia were
noted in one specimen, and seromucous glands were seen
to empty to the surface through both types of epithelia. In
H. sapiens, the only vestige of the NPD was a small fossa
located within an elongated recess (Fig. 3F), the nasopal-
Fig. 2. A: A coronal section showing the VNOs of a juvenile chimpanzee, which exhibit a spatial separation from the paraseptal cartilage (PC). B and C: The chimpanzee VNO had multiple glandular
communications (open arrows ⫽ glands; GD ⫽ gland duct; GL ⫽
gland) throughout most of the anteroposterior extent of the VNO (B ⫽
1st percentile; C ⫽ 50th percentile). In the left VNO of one specimen
(a juvenile chimpanzee) it was possible to observe cilia (open arrows)
and basal bodies (arrow heads) throughout the entire anteroposterior
extent (D ⫽ 75th percentile; E ⫽ 100th percentile). Basal cells (BCs)
were seen, and gaps in (D) basal bodies revealed goblet cells (GCs)
and at least one other nonciliated cell type. F: A coronal section
showing the location of the VNO in a 2-year-old human. G: VNO in a
77-year-old male. In some humans, a continuous row of cilia (open
arrows) could be seen on all inner surfaces of the VNO (G ⫽ 100 ␮m
posterior to the VNO opening in the subject shown), and numerous
glands (GLs) could be seen to empty into the VNO throughout most of
the anteroposterior extent (H ⫽ 50th percentile of same adult human).
I: In most humans, however, some nonciliated portions of the VNO
were seen, as shown in the 100th percentile of the VNO in the same
adult human. L ⫽ lumen of VNO; NS ⫽ nasal septum. Scale bars: A
and F ⫽ 600 ␮m; B, C, and H ⫽ 150 ␮m; D and G ⫽ 30 ␮m; E and I ⫽
40 ␮m.
172
SMITH ET AL.
Fig. 3. A: The region of the NPD in a neonatal Eulemur mongoz, just
posterior to its communication with the vomeronasal duct (*). A, B, and
D: The NPD was lined with stratified squamous epithelium in all strepsirhine species. B and C: An adult Otolemur crassicaudatus was unique
in possessing intraepithelial mucous glands (open arrows) in both the
vomeronasal duct and NPD. The vomeronasal duct of most species was
stratified cuboidal, as shown in (D) an infant Saguinus geoffroyi, although
Otolemur was unique in possessing vomeronasal ducts (*) mostly lined
with (C) a keratinized, stratified squamous epithelium. The NPD of the
chimpanzee was blind-ended, penetrating only partially through the
superior palate ((E) juvenile chimpanzee). The NPD of Pan troglodytes
was mostly lined with a stratified squamous epithelium that had numerous seromucous glands (open arrows) emptying through it (GD ⫽ gland
ducts). No NPD was found in humans ((F) 79-year-old male); there was
only a remnant in the form of a shallow groove, the NPR. The NPR was
lined with respiratory epithelium and had numerous seromucous glands
(open arrows) in the lamina propria. Scale bars: A and F ⫽ 600 ␮m; B and
E ⫽ 300 ␮m; C and D ⫽ 150 ␮m.
atine recess (NPR) (Bhatnagar and Smith, 2001). Both the
recess and fossa were lined with a highly glandular respiratory mucosa (Figs. 3F and 4H).
Glands associated with the VNO were PAS⫹ and AB– in
all strepsirhines examined, in both neonates and adults
(Fig. 4A and C), whereas glands not communicating with
the VNO lumen, but emptying into the nasal cavity directly, were AB⫹ and PAS⫹ (Fig. 4C). However, glands of
the vomeronasal duct were AB⫹/PAS⫹ in O. crassicaudatus (Fig. 4B). In all primates, unicellular glands lining the
nasal cavity (i.e., goblet cells) were AB⫹ and PAS⫹. In all
New World monkeys, H. sapiens, and P. troglodytes,
glands that communicated with the VNO were AB⫹/
PAS⫹, and some AB⫹ secretions were found in gland ducts
or the VNO itself (Fig. 4D–G, and K). In all species represented at different ages, subadults were relatively less
PRIMATE VOMERONASAL ORGAN AND NASOPALATINE DUCT
PAS⫹ compared to adults. Glands were most abundant
superiorly and posteriorly in S. geoffroyi and L. rosalia,
but were otherwise sparse; sparse goblet cells also were
seen, but not in all sections examined. Glands were similarly distributed and more abundant in C. jacchus. Unique
rostral glands were seen in A. caraya, which coursed posteriorly via large ducts that connected to the VNO at its
intersection with the NPD. Glands that emptied into the
VNO of H. sapiens and P. troglodytes also were AB⫹/
PAS⫹, including intraepithelial glands (Fig. 4G and K).
Glands associated with the nasopalatine region in H. sapiens and P. troglodytes were AB⫹/PAS⫹ (Fig. 4H–I). In
both H. sapiens and P. troglodytes, adult specimens had
more goblet cells and intraepithelial glands in the VNO
than juveniles. Numerous adult humans and the adult
chimpanzee had AB⫹/PAS⫹ material completely occluding
the VNO lumen at some anteroposterior levels. The sections that were soaked in diastase of malt prior to staining
still showed PAS positivity in all glands, indicating that
the PAS⫹ structures contained neutral mucins.
DISCUSSION
Bhatnagar and Smith (2001) described two functional
categories of VNOs: chemosensory and nonchemosensory.
Morphologically, there appear to be more categories, or
character states, of VNOs that may have phylogenetic,
rather than strictly functional, significance (Smith et al.,
2001a). VNOs of humans and chimpanzees are similar to
each other and histologically distinct from the chemosensory VNOs seen in strepsirhines. Unfortunately, the human/chimpanzee VNO is minute (approximately 2–12 mm
in length) and is more easily confused with other mucosal
structures compared to the chemosensory VNO of strepsirhines. Proportionately, adult VNO length ranged from
16.4% to 19.7% of head length in Microcebus murinus, but
from only 0.5% to 5.6% of head length in H. sapiens (Smith
et al., 2001d).
The VNO of humans and chimpanzees may be likened to
some aspects of other mucosal structures in the nasal
septum. For example, the human/chimpanzee VNO is similar to an exocrine gland duct in overall shape and because
of the multiple seromucous glands that empty into its
lumen. However, most seromucous gland ducts are nonciliated and simple cuboidal, and are not bilateral in nature (Smith et al., 2001a, b). The ciliated gland ducts
found in E. mongoz and other species are more similar (see
Fig. 6H in Smith et al., 2001a), but are unilateral structures found in variable locations. There are at least four
cell types in the human/chimpanzee VNO: basal cells,
ciliated cells, goblet cells, and at least one unidentified
type of nonciliated columnar cell. Indications of basal bodies suggest that motile cilia, rather than long microvilli (as
seen in the VNO of other mammals) or olfactory cilia (as
seen in the olfactory epithelium), exist in the human and
chimpanzee VNO. Although the embryogenesis of the
VNO in chimpanzees has not been described, in humans
the ontogeny of the VNO from a sensory structure (at 43
days to 12 weeks of embryonic development) to a duct-like,
ciliated structure (cilia first appearing at 10 weeks fertilization age) can be clearly traced (Boehm and Gasser,
1993; Smith and Bhatnagar, 2000). Variability in the extent of anteroposterior or right vs. left presence of cilia
among the few specimens examined emphasizes the need
for further ontogenetic study of cilia in the VNO in H.
sapiens and P. troglodytes. The ontogeny of the ciliated
duct in E. mongoz is unclear, but unless it originated from
173
the anterior part of the primordial VNO, it simply represents a functional analog of the human/chimpanzee VNO.
Ciliated gland ducts leading to the VNO in L. rosalia and
C. jacchus strengthen this view, and suggest a function in
secretion transport.
One similarity between the human/chimpanzee VNO
and that seen in other primates is in the vomeronasal
duct, which consists of stratified cuboidal epithelium in all
cases. The human and chimpanzee VNO may therefore be
regarded as having a short duct, followed by pseudostratified, columnar epithelium. A noteworthy aspect of this
duct in humans and chimpanzees is its glandular nature,
with both external and intraepithelial glands. Intraepithelial glands of similar histochemistry also were seen in
the vomeronasal duct of O. crassicaudatus. This presents
an interesting point of comparison since O. crassicaudatus
possesses the morphological structures (surrounding cartilaginous capsules, large venous sinuses) associated with
the “vasomotor pumping” mechanism (Meredith and
O’Connell, 1979) that is thought to aid VNO function
(Hedewig, 1980). Thus, these secretions could potentially
be drawn into the VNO in O. crassicaudatus and play a
role in VNO function. On the other hand, it is noteworthy
that these intraepithelial glands were histochemically
more similar to glands of the nasal cavity proper than to
the vomeronasal glands. It is therefore possible that they
produced accessory secretions released to the nasal or oral
cavities.
It has recently been suggested (Jacob et al., 2000; Bhatnagar and Smith, 2001; Smith et al., 2001c) that some
investigators attempting to study the human VNO have
inadvertently examined the NPD region (containing only
a small pit) rather than the VNO itself, as there are
histological similarities between the two regions (Bhatnagar and Smith, 2001). This confusion may have occurred
in H. sapiens, but there are clear distinctions between the
human/chimpanzee VNO and the NPD of primates in
general. The NPD, where present, shows adaptations for
transport of substances between the oral and nasal cavities, and also to or from the VNO duct. In contrast, the
nasopalatine region of P. troglodytes (blind-ended duct)
and H. sapiens (minute pit) appears to provide accessory
glandular tissue, unlike the other species examined (with
the exception of O. crassicaudatus). The literature does
not support the suggestion that only glands secreting neutral mucins are compatible with functional VNOs (e.g., see
Salazar et al., 1997). However, the histochemical partitioning of neutral mucin secretions to the VNO and acidic/
neutral secretions to the remainder of the nasal cavity is
striking in strepsirhines (and other mammals (see Roslinski et al., 2000)). In contrast, the VNO of New World
monkeys was histochemically more similar to H. sapiens
and P. troglodytes than to the strepsirhines, which may
reflect general similarities among haplorhine primates.
With the above features in mind, the VNO of humans
and chimpanzees is defined by a suite of characteristics, as
is the strepsirhine VNO. There is little overlap between
these characteristics, rendering them useful character
states. In order to exclude some similarities to seromucous
gland ducts or specialized ciliated ducts, VNOs of H. sapiens and P. troglodytes are regarded as paired structures
that are 1) bilateral epithelial tubes; 2) in a superiorly
displaced position in the same plane as the paraseptal
cartilages; 3) lined with a homogeneous, pseudostratified
columnar morphology with ciliated regions; and 4) have
internal mucous-producing structures (i.e., contain goblet
174
SMITH ET AL.
Figure 4.
PRIMATE VOMERONASAL ORGAN AND NASOPALATINE DUCT
175
Fig. 4. Histochemical variation of the vomeronasal and nasopalatine regions using AB-PAS staining, revealing acidic (AB) and neutral (PAS)
mucins. A: A slightly oblique coronal section from a neonatal primate (Galago moholi) showing the NPD just posterior to the VNO opening, with the
vomeronasal duct on the left side of the image and the VNO on the right side of the image. Note the absence of any AB⫹ (blue) stain adjacent to
the VNO or its duct. B: A magnified coronal section showing the communication of the NPD to the VNO duct (open arrow) in an adult Otolemur
crassicaudatus. Note the AB⫹ glands lining the ducts, which were unique in the species among strepsirhines. C: The VNO is shown in an adult
Otolemur crassicaudatus. Note the PAS⫹ glands (open arrows) around the VNO, whereas the AB⫹ glands (small arrows) are found elsewhere, e.g.,
goblet cells along the respiratory epithelium. D: A neonatal Leontopithecus rosalia showing primarily AB⫹ glands communicating to the VNO; no
glands were associated with the NPD. E: A 4-month-old L. rosalia showed somewhat more numerous AB⫹ (small arrows) and PAS⫹ (open arrow)
glands, along with secretions in the lumen. F: The VNO of Callithrix jacchus showed more extensive AB⫹ glands than other callitrichids, shown here
superior to the VNOs (small arrows). The (G) VNO and (H) NPR (a vestige of the duct) from a 2-year-old human are shown. I: The inset shows both
regions and the distance between them. Note that the VNO has predominantly AB⫹ glands (G), whereas the NPR has both AB⫹ (small arrow) and
PAS⫹ (open arrow) glands. The blind-ended NPD remnant (J) and VNO (K) of a juvenile chimpanzee had AB⫹ glands. L ⫽ VNO lumen; NPD ⫽
nasopalatine duct; NPR ⫽ nasopalatine recess; NS ⫽ nasal septum; PC ⫽ paraseptal cartilage; VNC ⫽ vomeronasal cartilage. Scale bars: A–D ⫽
300 ␮m; E and F ⫽ 150 ␮m; G and H ⫽ 600 ␮m; I ⫽ 800 ␮m; J ⫽ 300 ␮m; K ⫽ 150 ␮m.
cells or multicellular intraepithelial glands). It is possible
to speculate that this character state may properly be
regarded as a synapomorphic condition of hominoids, especially since epithelial tubes that are positionally similar
to the human VNO have been located in orangutan and
gorilla fetuses (C.S. Evans, personal communication).
Functionally, this structure remains poorly understood,
but highly distinctive aspects of the VNOs of humans and
chimpanzees compared to other primates appear to indicate accessory glandular activity at minimum. The sparse,
unidentified nonciliated cells seen in humans and chimpanzees offer little basis for speculation on their chemosensory function, especially in the absence of adjacent
unmyelinated axons. Some such cells were roughly “receptor-like” in shape (e.g., in a chimpanzee (Fig. 1K)), yet
these also may represent populations of other cells (such
as leukocytes) known to occur in the NSE of the mammalian VNO (Adams and Weikamp, 1984; Carmanchahi et
al., 1999). There is clearly a need to examine larger samples of fresh tissue from hominoids to gather immunohistochemical or electron microscopic data to clarify the identity of such cells. The data of the present study are limited
in regard to functional interpretation, but may be in keeping with known trends regarding the central connection of
the VNO in primates, the accessory olfactory bulb. The
accessory olfactory bulb is absolutely and proportionately
largest in strepsirhines, smaller in New World primates
(Stephan et al., 1982), and only present prenatally in Old
World primates (see Bhatnagar and Meisami, 1998; Meisami and Bhatnagar, 1998); the degree of neuroepithelial
presence among primates in the present study appeared to
correspond to those data. Interestingly, there also appeared to be a difference in the amount of VNNE in the
neonatal strepsirhines compared to that in the two neonatal callitrichids (see also Evans and Grigorieva, 1994),
although glandular development was incomplete at birth
in all neonates.
Previous efforts to locate a VNO in postnatal Old World
primates may have been hampered by the expectation
that the VNOs of Old World species would be located in a
position similar to those of strepsirhines and New World
species (i.e., near the palate, surrounded by vomeronasal
cartilages). It is now clear that the VNO of humans and
chimpanzees is positionally and histologically different
from that of other primates; developmental evidence indicates that they are homologous structures (Starck, 1960;
Smith and Bhatnagar, 2000)1. Recent attempts to find
similar structures in postnatal Colobus guereza (Smith et
al., 2001b) and Macaca spp. (Smith et al., 2001a), suggest
that Cercopithecoids may lack the VNO postnatally (Jordan, 1972). It is necessary to reexamine the VNO using a
broad spectrum of haplorhine primates, keeping in mind
the unique character states exhibited by hominoids and
New World monkeys.
ACKNOWLEDGMENTS
We are grateful to A.B. Taylor for arranging access to
the marmoset tissues used in this study. All procedures
related to processing the human material used for this
study were reviewed and approved by the Human Studies
Committee, Department of Anatomical Sciences and Neurobiology, University of Louisville, and the Institutional
Review Board for the Protection of Human Subjects, Slippery Rock University. This is Duke University Primate
Center publication #747.
LITERATURE CITED
Adams DR, Wiekamp MD. 1984. The canine vomeronasal organ. J
Anat 138:771–787.
Ankel-Simons F. 2000. Primate anatomy: an introduction. New York:
Academic Press. 506 p.
Bhatnagar KP, Meisami E. 1998. Vomeronasal organ in bats and
primates: extremes of structural variability and its phylogenetic
implications. Microsc Res Technol 43:465– 475.
Bhatnagar KP, Smith TD. 2001. The human vomeronasal organ. Part
III. Postnatal development from infancy to the ninth decade. J Anat
199:289 –302.
Boehm N, Gasser B. 1993. Sensory receptor-like cells in the human
foetal vomeronasal organ. NeuroReport 4:867– 870.
Breipohl W, Bhatnagar KP, Mendoza A. 1979. Fine structure of the
receptor-free epithelium in the vomeronasal organ of the rat. Cell
Tissue Res 200:383–395.
Carmanchahi PD, Aldana Marcos HJ, Ferrari CC, Affani JM. 1999.
The vomeronasal organ of the South American armadillo Chaetophractus villosus (Xenarthra, Mammalia): anatomy histology and
ultrastructure. J Anat 195:587– 604.
1
The existing evidence for homology of the human VNO (Smith
and Bhatanagar, 2000) is stronger than that for the chimpanzee,
and there is clearly a need for a careful embryologic study of the
VNO region in Pan troglodytes. It is noteworthy, however, that
Starck (1960) described VNO-like structures in a fetal chimpanzee that appeared to be nearly identical to that of fetal humans.
176
SMITH ET AL.
Ciges M, Labella T, Gayoso M, Sanchez G. 1977. Ultrastructure of the
organ of Jacobson and comparative study with olfactory mucosa.
Acta Otolaryngol 83:47–58.
Evans CS, Grigorieva EF. 1994. Morphology of the vomeronasal organ
in two South American monkeys (Saguinus labiatus and Cebuella
pygmaea, Callitrichidae): histology and lectin histochemistry. Adv
Biosci 93:31– 42.
Grosser BI, Monti-Bloch L, Jennings-White C, Berliner DL. 2000.
Behavioral and electrophysiological effects of androstadienone, a
human pheromone. Psychoneuroendocrinol 25:289 –299.
Hedewig R. 1980. Vergleichende anatomische untersuchungen an den
Jacobsonschen organen von Nycticebus coucang and Galago crassicaudatus. E. Geoffroy, 1812 (Prosimiae, Lorisidae). II. Teil: Galago
crassicaudatus. Morphol Jahrb 126:676 –722.
Humason G. 1979. Animal tissue techniques. San Francisco: W.H.
Freeman and Co. 661 p.
Hunter AJ, Fleming D, Dixon AF. 1984. The structure of the vomeronasal organ and nasopalatine ducts in Aotus trivirgatus and some
other primate species. J Anat 138:217–225.
Jacob S, Zelano B, Gungor A, Abbott D, Naclerio R, McClintock MK.
2000. Location and gross morphology of the nasopalatine duct in
human adults. Arch Otolaryngol Head Neck Surg 126:741–748.
Johnson A, Josephson R, Hawke M. 1985. Clinical and histological
evidence for the presence of the vomeronasal (Jacobson’s) organ in
adult humans. J Otolaryngol 14:71–79.
Jordan J. 1972. The vomeronasal organ (of Jacobson) in primates.
Folia Morphol (Warsz) 31:418 – 432.
Kölliker A. 1877. Ueber die Jacobson’schen Organe des Menschen. In:
F. von Rinecker, Festschrift. Wilhelm Engelmann: Leipzig. p 3–11.
Kouros-Mehr H, Pintchovski S, Melnyk K, Yu-Jiun C, Friedman C,
Trask B, Shizuya H. 2001. Identification of non-functional human
VNO receptor genes provides evidence for vestigiality of the human
VNO. Chem Senses 26:1167–1174.
Loo S. 1973. A comparative study of the nasal fossa of four nonhuman
primates. Folia Primatol 20:410 – 422.
Meisami E, Bhatnagar KP. 1998. Structure and diversity in mammalian accessory olfactory bulb. Microsc Res Technol 43:476 – 499.
Meredith M, O’Connell RJ. 1979. Efferent control of stimulus access to
the hamster vomeronasal organ. J Physiol 286:301–316.
Nowak RM. 1999. Walker’s primates of the world. Baltimore: Johns
Hopkins University Press. 224 p.
Potiquet M. 1891. Du canal de Jacobson. Rev Laryngol D’Otol Rhinol
2:737–753.
Roslinski DL, Bhatnagar KP, Burrows AM, Smith TD. 2000. Comparative morphology and histochemistry of glands associated with the
vomeronasal organ in humans, mouse lemurs, and voles. Anat Rec
260:92–101.
Salazar I, Quinteiro PS, Cifuentes JM. 1997. The soft-tissue components of the vomeronasal organ in pigs, cows, and horses. Anat
Histol Embryol 26:179 –186.
Smith TD, Siegel MI, Burrows AM, Mooney MP, Burdi AR, Fabrizio
PA, Clemente FR. 1998. Searching for the vomeronasal organ of
adult humans: preliminary findings on location, structure, and size.
Microsc Res Technol 41:483– 491.
Smith TD, Bhatnagar KP. 2000. The human vomeronasal organ. Part
II. Prenatal development. J Anat 197:421– 436.
Smith TD, Siegel MI, Bhatnagar KP. 2001a. Reappraisal of the vomeronasal system of catarrhine primates: ontogeny, morphology, functionality, and persisting questions. Anat Rec (New Anat) 265:176 –
192.
Smith TD, Siegel MI, Bonar CJ, Bhatnagar KP, Mooney MP, Burrows
AM, Smith MA, Maico LM. 2001b. The existence of the vomeronasal
organ in postnatal chimpanzees and evidence for its homology with
that of humans. J Anat 198:77– 82.
Smith TD, Buttery TA, Bhatnagar KP, Burrows AM, Mooney MP,
Siegel MI. 2001c. Anatomical position of the vomeronasal organ in
postnatal humans. Ann Anat 183:415– 479.
Smith TD, Mooney MP, Burrows AM, Bhatnagar KP, Siegel MI.
2001d. Prenatal growth and adult size of the vomeronasal organ in
mouse lemurs and humans. In: Marchlewska A, Lepri JJ, MullerSchwartze D, editors. Chemical signals in vertebrates. Vol. IX. New
York: Kluwer Academic/Plenum Press. p 93–99.
Starck D. 1960. Das Cranium eines Schimpansenfetus (Pan troglodytes [Blumenbach 1799]) von 71 mm SchStlg., nebst Bemerkungen
über die Körperform von Schimpansenfeten. Morphol Jahrb 100:
559 – 647.
Stephan H, Baron G, Frahm HD. 1982. Comparison of brain structure
volumes in Insectivora and Primates. II. Accessory olfactory bulb
(AOB). J Hirnforsch 23:575–591.
Wysocki CJ, Preti G. 2000. Human body odors and their perception.
Jpn J Smell Taste Res 7:19 – 42.
Zingeser MR. 1984. The nasopalatine ducts and associated structures
in the rhesus monkey (Macaca mulatta): topography, prenatal development, function, and phylogeny. Am J Anat 170:581–595.
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