Dopaminergic modulation of olfactory-evoked motor output in sea lampreys (Petromyzon marinus L.).

Philippe‐Antoine Beauséjour,François Auclair,Gheylen Daghfous,Barbara Zielinski,Réjean Dubuc,Danielle Veilleux,Catherine Ngovandan

doi:10.1002/cne.24743

Philippe‐Antoine Beauséjour, François Auclair + Show 5 more

Open Access

https://doi.org/10.1002/cne.24743

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Abstract

Detection of chemical cues is important to guide locomotion in association with feeding and sexual behavior. Two neural pathways responsible for odor‐evoked locomotion have been characterized in the sea lamprey (Petromyzon marinus L.), a basal vertebrate. There is a medial pathway originating in the medial olfactory bulb (OB) and a lateral pathway originating from the rest of the OB. These olfactomotor pathways are present throughout the life cycle of lampreys, but olfactory‐driven behaviors differ according to the developmental stage. Among possible mechanisms, dopaminergic (DA) modulation in the OB might explain the behavioral changes. Here, we examined DA modulation of olfactory transmission in lampreys. Immunofluorescence against DA revealed immunoreactivity in the OB that was denser in the medial part (medOB), where processes were observed close to primary olfactory afferents and projection neurons. Dopaminergic neurons labeled by tracer injections in the medOB were located in the OB, the posterior tuberculum, and the dorsal hypothalamic nucleus, suggesting the presence of both intrinsic and extrinsic DA innervation. Electrical stimulation of the olfactory nerve in an in vitro whole‐brain preparation elicited synaptic responses in reticulospinal cells that were modulated by DA. Local injection of DA agonists in the medOB decreased the reticulospinal cell responses whereas the D2 receptor antagonist raclopride increased the response amplitude. These observations suggest that DA in the medOB could modulate odor‐evoked locomotion. Altogether, these results show the presence of a DA innervation within the medOB that may play a role in modulating olfactory inputs to the motor command system of lampreys.

Highlights

Lampreys represent the oldest extant group of vertebrates and their behavior is strongly influenced by olfactory inputs
When dopamine (DA) and gabazine are simultaneously injected in the medial part of the olfactory bulbs (OB) (medOB), the mean response amplitude is significantly decreased (n = 5 cells in five larvae). (b) Mean response amplitudes during each condition are plotted as a line graph for every recorded RS cell. (c) Illustrates a representative example of RS cell subthreshold responses under control conditions (c1), gabazine injection (c2), gabazine and DA injection (c3), and after washout of DA but still under gabazine (c4)
Local injection of gabazine in the medOB amplifies RS cell synaptic responses, a combined DA injection induces a marked decrease of these subthreshold (c) or suprathreshold (d) responses, which is reversed after washout of DA

Summary

Introduction

Lampreys represent the oldest extant group of vertebrates and their behavior is strongly influenced by olfactory inputs. Sea lampreys (Petromyzon marinus L.) rely heavily on the detection of chemical cues for feeding (Kleerekoper & Mogensen, 1963) and sexual behaviors (Buchinger, Siefkes, Zielinski, Brant, & Li, 2015). As odorant perfusion on the olfactory epithelium of lampreys from prolarval (Zielinski, Fredricks, Mcdonald, & Zaidi, 2005) to spawning (Li, Sørensen, & Gallaher, 1995) stages activates sensory neurons, olfaction is thought to induce motor behavior throughout life. Compared to other vertebrate species, lampreys have a large proportion of their brain dedicated to processing olfactory inputs, the size of the olfactory bulbs (OB) even exceeding that of the cerebral hemispheres (Nieuwenhuys, 1977). Secondary olfactory neurons have extensive projections throughout the prosencephalon (Northcutt & Puzdrowski, 1988)

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