Connectivity from OR37 expressing olfactory sensory neurons to distinct cell types in the hypothalamus

Abstract

Olfactory sensory neurons (OSNs) which express a member from the OR37 subfamily of odorant receptor (OR) genes are wired to the main olfactory bulb (MOB) in a unique monoglomerular fashion; from these glomeruli an untypical connectivity into higher brain centers exists. In the present study we have investigated by DiI and transsynaptic tracing approaches how the connection pattern from these glomeruli into distinct hypothalamic nuclei is organized. The application of DiI onto the ventral domain of the bulb which harbors the OR37 glomeruli resulted in the labeling of fibers within the paraventricular nucleus (PVN) and supraoptic nucleus (SO) of the hypothalamus; some of these fibers were covered with varicose-like structures. No DiI-labeled cell somata were detectable in these nuclei. The data indicate that projection neurons which originate in the OR37 region of the MOB form direct connections into these nuclei. The cells that were labeled by the transsynaptic tracer WGA in these nuclei were further characterized. Their distribution pattern in the paraventricular nucleus was reminiscent of cells which produce distinct neuropeptides. Double labeling experiments confirmed that they contained vasopressin, but not the related neuropeptide oxytocin. Morphological analysis revealed that they comprise of magno- and parvocellular cells. A comparative investigation of the WGA-positive cells in the SO demonstrated that these were vasopressin-positive, as well, whereas oxytocin-producing cells of this nucleus also contained no transsynaptic tracer. Together, the data demonstrates a connectivity from OR37 expressing sensory neurons to distinct hypothalamic neurons with the same neuropeptide content.

Neuromodulation by oxytocin and vasopressin in the central nervous system as a basis for their rapid behavioral effects

“…In addition, previous electrophysiological findings revealed monosynaptic afferents from the olfactory system onto the SON [15] and more recently, direct projections from the MOB glomeruli onto VP containing neurons in both PVN and SON. Interestingly, these glomeruli are innervated by a subset of OR-37 receptor expressing olfactory neurons that are implicated in detecting socially relevant chemical signals [16].…”

The Evolving Neural and Genetic Architecture of Vertebrate Olfaction

“…Together these data suggest that humans may still detect a set of informative odors through the OR37 family, such as the long-chain fatty aldehyde ligands sensed by mouse OR37 members [73]. Intriguingly, mouse mitral cell projections from OR37 glomeruli target several hypothalamic nuclei rather than the cortical regions typical of most main olfactory bulb projections (Figure 5) [74, 75]. Thus the OR37 family may have evolved to link the sensation of a certain chemical class to regulation of innate behaviors or internal state in a way that has remained crucial across species.…”

“…First, an “innate aversion” domain for predator odor sensation can be found at the ventral subdivision of the dorsal olfactory bulb, while the dorsal-most Class I-expressing domain is instead required for aversive responses to spoiled food odorants [108]. Next, the ventral olfactory bulb houses the glomeruli of molecularly distinct neurons (expressing components of an alternative, TrpM5-dependent chemotransduction pathway) that preferentially respond to urine-derived pheromones and project to the “vomeronasal amygdala”, as well as the cluster of OR37 glomeruli and their unusual mitral cell projections to the hypothalamus [75, 77, 109, 110]. Finally, the TAAR domain of the olfactory bulb is required for innate behavioral responses to several ecologically important amines, even though these same odorants can be detected by receptors in the main olfactory system (Figure 5) [84].…”

Central Nervous System Control of Oxytocin Secretion during Lactation

“…The olfactory bulb has projections to the hypothalamus, 192,193 clearly plays a role in maternal behavior, 194 and shows c-Fos activation at parturition. 195 It has been speculated that mitral cells directly innervate neurosecretory neurons in the SON.…”