Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status

Abstract

BackgroundOlfaction is a fundamental sense through which most animals perceive the external world. The olfactory system detects odors via specialized sensory organs such as the main olfactory epithelium and the vomeronasal organ. Sensory neurons in these organs use G-protein coupled receptors to detect chemosensory stimuli. The odorant receptor (OR) family is expressed in sensory neurons of the main olfactory epithelium, while the adult vomeronasal organ is thought to express other types of receptors.ResultsHere, we describe Olfr692, a member of the OR gene family identified by next-generation RNA sequencing, which is highly upregulated and non-canonically expressed in the vomeronasal organ. We show that neurons expressing this gene are activated by odors emanating from pups. Surprisingly, activity in Olfr692-positive cells is sexually dimorphic, being very low in females. Our results also show that juvenile odors activate a large number of Olfr692 vomeronasal neurons in virgin males, which is correlated with the display of infanticide behavior. . In contrast, activity substantially decreases in parenting males (fathers), where infanticidal aggressive behavior is not frequently observed.ConclusionsOur results describe, for the first time, a sensory neural population with a specific molecular identity involved in the detection of pup odors. Moreover, it is one of the first reports of a group of sensory neurons the activity of which is sexually dimorphic and depends on social status. Our data suggest that the Olfr692 population is involved in mediating pup-oriented behaviors in mice.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0234-9) contains supplementary material, which is available to authorized users.

Olfactory and Vomeronasal Receptor Feedback Employ Divergent Mechanisms of PERK Activation

“…Substitution of an OR coding sequence with a VR and vice versa would result in UPR induction in both types of sensory neurons. However, prolonged UPR activation would result in stable receptor expression only in VSNs, in agreement with the outcomes of these substitution experiments 20,32,44 and in agreement with the demonstration that Olfr692 is expressed in the VNO 45 . It therefore appears that, unlike in OSNs, termination of ATF5 translation is not required for stabilization of VR expression.…”

The Role of Olfactory Genes in the Expression of Rodent Paternal Care Behavior

“…The nose houses the MOS, which consists of the main olfactory epithelium (MOE; Figure 1). This is the primary site for the detection of volatile odorants [1]. The main olfactory sensory neurons (OSNs) in the MOE, of which there are approximately 10 million in vertebrates, are located directly in the nasal airstream; thus, stimulus access simply requires passive respiration or a sniffing action [34].…”

“…The main olfactory sensory neurons (OSNs) in the MOE, of which there are approximately 10 million in vertebrates, are located directly in the nasal airstream; thus, stimulus access simply requires passive respiration or a sniffing action [34]. The 500-1000 olfactory receptors (ORs [1,27,35]) that belong to the rhodopsin-like G-protein-coupled receptor superfamily (GPCRs [26,35,36]), are located in the cell membranes of the OSNs, and bind specific odorant ligands [35]. While the ORs are responsible for detecting chemosensory cues, they are also involved in axonal guidance to the brain [36,37].…”

“…Olfr692 is a member of the OR gene family that is highly expressed in the basal zone of the VNO (Table 1) of adult male mice [1,110], with expression levels similar to those of Vmn1r188 and Vmn2r118 in the V1R and V2R families [1]. An extensive number of Olfr692-positive cells occurs in the VNOs of adult rodents, but expression is virtually absent in juveniles [1].…”

“…In order to survive, all animals must detect, interpret and respond to an array of sensory information in their immediate environment [1]. Animals need to locate and assess the quality of food, detect and avoid predators, and identify mates and competitors [1]. Animals can gain information about these resources or threats, as well as convey information to other individuals, via numerous modalities, including vision and olfaction.…”