Expression of neuron‐specific markers by the vomeronasal neuroepithelium in six species of primates

Abstract

Vomeronasal organ (VNO) morphology varies markedly across primate taxa. Old World monkeys display no postnatal VNO. Humans and at least some apes retain a vestigial VNO during postnatal life, whereas the strepsirrhines and New World Monkeys present a morphologically well-defined VNO that, in many species, is presumed to function as an olfactory organ. Available microanatomical and behavioral studies suggest that VNO function in these species does not precisely duplicate that described in other mammalian taxa. The questions of which species retain a functional VNO and what functions they serve require inquiry along diverse lines but, to be functional, the vomeronasal epithelium must be neuronal and olfactory. We used immunohistochemistry to establish these criteria in six primate species. We compared the expression of two neuronal markers, neuron-specific ␤-tubulin (BT) and protein gene product 9.5, and olfactory marker protein (OMP), a marker of mature olfactory sensory neurons, in paraffin-embedded VNO sections from two strepsirrhine and four haplorhine species, all of which retain morphologically well-defined VNOs during postnatal life. The infant Eulemur mongoz, adult Otolemur crassicaudatus, neonatal Leontopithicus rosalia, and adult Callithrix jacchus express all three proteins in their well-defined vomeronasal neuroepithelia. The infant Tarsius syrichta showed some BT and OMP immunoreactivity. We establish that two strepsirrhine species and at least some New World haplorhines have mature sensory neurons in the VNO. In contrast, at all ages examined, Saguinus geoffroyi VNO expresses these markers in only a few cells. © 2004 Wiley-Liss, Inc.Key words: immunohistochemistry; olfaction; olfactory marker protein; primate; ␤-tubulin; PGP 9.5; vomeronasalThe tetrapod vomeronasal organ (VNO) is bilaterally symmetric and lies along the ventrorostral aspect of the nasal septum. Sensory neurons in the vomeronasal neuroepithelium (VNNE) of snakes, rodents, and opossums detect chemical signals that evoke behavioral and/or physiological changes regarding prey identification, social status, and reproductive state (Wysocki, 1979;Halpern, 1987;Takami, 2002;Halpern and Martínez-Marcos, 2003).The rodent VNO is the best studied in terms of gene expression during development, its morphological organization, its secondary and higher-order connections, and its effects on the organism's behavior and physiology. For some time, the rodent VNO was thought to epitomize the mammalian vomeronasal system but VNO function as exemplified in rodents is not precisely replicated in other mammalian taxa, namely, ferrets (Weiler et al., 1999;

The vomeronasal organ of greater bushbabies (Otolemur spp.): Species, sex, and age differences

“…Recent immunohistochemical findings indicate that representatives of the two infraorders of Strepsirrhini, Lemuriformes and Lorisiformes, possess VNOs that express OMP (Dennis et al, 2004), a neuronal marker of mature olfactory and vomeronasal neurons (Farbman & Margolis, 1980;Margolis, 1980). Dennis et al (2004) also demonstrated that OMP was expressed at birth in species of the lemuriform genus Eulemur. The findings of the present study suggest this is also true of the lorisiform Otolemur garnettii.…”

“…Dennis et al (2004) hypothesized that, with regard to BT and OMP expression, primate vomeronasal sensory neurons follow a developmental program similar to that of sensory neurons of the rat main olfactory epithelium. In those cells, BT is expressed first followed by OMP expression and a down regulation of BT in the cell body (Lee & Pixley, 1994).…”

“…To that end, the present study examines size and neuronal marker expression in the VNNE of greater bushbabies (Otolemur crassicaudatus and O. garnettii), nocturnal strepsirrhines that rely heavily on chemosensory modes of communication (Eaton et al, 1973;Watson et al, 1999). This genus was selected because it was previously noted to possess well-developed VNOs (Dennis et al, 2004;Hedewig, 1980a), and a dispersed multi-male social system (Müller & Thalmann, 2000;Nash & Harcourt, 1986). The polygamous mating behavior typified by this social system was identified previously as a possible correlate of sexual dimorphism in the VNO (Maico et al, 2003;Tai et al, 2004).…”

Comparative study of lectin reactivity in the vomeronasal organ of human and nonhuman primates

“…While the significance of this difference is presently unclear, it may relate to different characteristics of the neuronal populations recently described for marmosets and tamarins. In fact, S. geoffroyi may have nonfunctional VNOs as adults based on the near absence of olfactory marker protein (OMP) expression in the VNO epithelium; OMP is ubiquitously present in the VNNE of C. jacchus (Dennis et al, 2004).…”

Olfactory fossa of Tremacebus harringtoni (platyrrhini, early Miocene, Sacanana, Argentina): Implications for activity pattern

“…The organ and bulb are smaller and extremely variable in platyrrhines (Stephan et al, 1981Baron et al, 1983;Dennis et al, 2004) and rudimentary in adult catarrhines (Stephan et al, 1981Baron et al, 1983). This suggests that pheromonal communication may not be as important to platyrrhines compared to strepsirrhines and may be even less important in catarrhines than in platyrrhines.…”