Olfactory Projections to Locomotor Control Centers in the Sea Lamprey

Although olfaction is well known to guide animal behavior, the neural circuits underlying the motor responses elicited by olfactory inputs are poorly understood. In the sea lamprey, anatomical evidence shows that olfactory inputs project to the posterior tuberculum (PT), a structure containing dopaminergic (DA) neurons homologous to the mammalian ventral tegmental area and the substantia nigra pars compacta. Olfactory inputs travel directly from the medial olfactory bulb (medOB) or indirectly through the main olfactory bulb and the lateral pallium (LPal). Here, we characterized the transmission of olfactory inputs to the PT in the sea lamprey, Petromyzon marinus. Abundant projections from the medOB were observed close to DA neurons of the PT. Moreover, electrophysiological experiments revealed that PT neurons are activated by both the medOB and LPal, and calcium imaging indicated that the olfactory signal is then relayed to the mesencephalic locomotor region to initiate locomotion. In semi-intact preparations, stimulation of the medOB and LPal induced locomotion that was tightly associated with neural activity in the PT. Moreover, PT neurons were active throughout spontaneously occurring locomotor bouts. Altogether, our observations suggest that the medOB and LPal convey olfactory inputs to DA neurons of the PT, which in turn activate the brainstem motor command system to elicit locomotion.