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

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.

Heterogeneous expression of dopaminergic markers and Vglut2 in mouse mesodiencephalic dopaminergic nuclei A8–A13

“…Second, in the ventral hypothalamus, a potential homolog to A11 comprises periventricular DA‐positive neurons projecting to the spinal cord (Barreiro‐Iglesias et al, 2008), but not to the mesencephalic locomotor region (Ryczko et al, 2013). Third, DA‐positive neurons of the dorsal hypothalamus project to the olfactory bulb, but their homolog in mammals is unresolved (Beauséjour et al, 2020). Fourth, DA‐positive neurons in the lamprey olfactory bulb are likely homolog to A16 (Beauséjour et al, 2020).…”

“…First, lamprey DA neurons located in the posterior tuberculum, a ventral diencephalic region, share similarities with mammalian A8–A10 DA neurons. These DA‐positive neurons project up to the striatum (Ericsson et al, 2013; Pombal, El Manira, & Grillner, 1997; Robertson et al, 2012; Ryczko et al, 2013; Stephenson‐Jones, Samuelsson, Ericsson, Robertson, & Grillner, 2011; von Twickel et al, 2019), olfactory bulb (Beauséjour et al, 2020), or down to the mesencephalic locomotor region (Ryczko et al, 2013), optic tectum (inferior colliculus in mammals, von Twickel et al, 2019), but not to the spinal cord (Ryczko et al, 2013). Some DA neurons contain glutamate and send functional glutamatergic inputs to their targets (Ryczko et al, 2017; von Twickel et al, 2019).…”

“…Third, DA‐positive neurons of the dorsal hypothalamus project to the olfactory bulb, but their homolog in mammals is unresolved (Beauséjour et al, 2020). Fourth, DA‐positive neurons in the lamprey olfactory bulb are likely homolog to A16 (Beauséjour et al, 2020). It would be interesting to determine whether lamprey DA neurons in the ventral and dorsal hypothalamus and olfactory bulb express DAT, glutamatergic, or GABAergic markers.…”

Expression of Urocortin 3 mRNA in the Central Nervous System of the Sea Lamprey Petromyzon marinus

“…Equivalences between these prosocial centers in mice with lamprey centers have yet to be reported, and the social life of lampreys is poorly known. Interestingly, the lamprey striatum, as the mouse medial amygdala, receives secondary olfactory projections [45,54], which might be important in mature adults for feeding, reproduction and mate choosing [55]. Recent studies of the olfactory system in the sea lamprey revealed two olfactory pathways via the medial and non-medial parts of the olfactory bulb that project toward the posterior tubercle and motor centers, and to the lateral pallium, respectively [56,57], but a direct relation of these medial and non-medial pathways with the striatum has yet to be deciphered.…”

The Dopaminergic Control of Movement-Evolutionary Considerations

“…The SNc/VTA also receives sensory information from multiple areas. Olfactory information reaches the SNc/VTA from both the medial olfactory bulb [ 46 ], a projection shown to contribute to locomotion [ 47 , 48 ], and from the main olfactory bulb [ 49 ]. Visual inputs reach the SNc/VTA from the tectum (homologue of the mammalian superior colliculus; SC), as well as the pretectum [ 3 , 8 , 50 ].…”