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The Neural Link between Novel Olfactory Signals and Locomotion
Barbara Zielinski1,2 and Réjean Dubuc3,4
1Department of Biological Sciences, University of Windsor, Windsor, Ontario.
2Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario.
3Groupe de Recherche en Activité Physique Adaptée (GRAPA), Département des Sciences de l’Activité Physique, Université du Québec à Montréal, Montréal, Québec.
4Groupe de Recherche sur le Système Nerveux Central (GRSNC), Département de Neurosciences, Université de Montréal,
The sea lamprey life cycle is heavily dependent on chemoreception, as feeding, migratory, and reproductive behaviors are driven by chemical cues. Under previous GLFC funding, we characterized a specific neural pathway linking olfactory and motor brain centers in lampreys. It extends from the medial part of the olfactory bulb (OB) to the mesencephalic locomotor region, with a single relay in the posterior tuberculum . Modulatory mechanisms acting on this pathway may account for the variability of lampreys’ behavioral responses to olfactory inputs . During the granting period, we focused our investigation on responses of olfactory sensory neurons (OSNs), olfactory bulb (olfactory integration) and reticulospinal neurons (motor control) to semiochemicals including pheromones and combinations of these compounds. The newly discovered phermone DKPES and its combination with the well-characterized 3kPZS were of particular interest for our study. However, we also tested PZS, PSDS, PAMS-24, compound 971, compound 973, as well as the two polyamines spermine and spermidine. Using electrophysiological and imaging techniques we showed that DKPES alone could activate the olfacto-motor circuitry all the way down to the reticulospinal system. However, the most potent responses were seen when it was combined with 3kPZS. Calcium imaging of the olfactory epithelium further showed that lamprey OSNs were narrowly-tuned and responded only to one odorant. OSNs responding to a particular odorant were intermingled with OSNs responding to other odorants. This is consistent with results from in situ experiments that showed that chemosensory receptors 6425.OR and 3721.TAAR are expressed in OSNs widely distributed in the main olfactory epithelium (i.e. we did not observe any segregation in their distribution). A series of electrophysiological and neuroanatomical experiments showed that olfactory inputs are processed by two parallel neural pathways from these sensory neurons to brainstem locomotor centers. These two pathways are strongly modulated by GABA, 5-HT, and Dopamine. Moreover, we found that olfactory bulb responses to pheromones are modulated by hormonal changes. Taken together, our results show that olfactomotor responses can be potentiated by using mixtures ofolfactory-stimulating compounds but also by using neuromodulators acting on the pathways we have identified.