Restricted co‐localization of glutamate and dopamine in neurons of the adult sea lamprey brain

Abstract

Co-localization of dopamine with other classical neurotransmitters in the same neuron is a common phenomenon in the brain of vertebrates. In mammals, some dopaminergic neurons of the ventral tegmental area and the hypothalamus have a glutamatergic co-phenotype. However, information on the presence of this type of dopaminergic neurons in other vertebrate groups is very scant. Here, we aimed to provide new insights on the evolution of this neuronal co-phenotype by studying the presence of a dual dopaminergic/glutamatergic neuron phenotype in the central nervous system of lampreys. Double immunofluorescence experiments for dopamine and glutamate in adult sea lampreys revealed co-localization of both neurotransmitters in some neurons of the preoptic nucleus, the nucleus of the postoptic commissure, the dorsal hypothalamus and in cerebrospinal fluid-contacting cells of the caudal rhombencephalon and rostral spinal cord. Moreover, co-localization of dopamine and glutamate was found in dopaminergic fibres in a few brain regions including the lateral pallium, striatum, and the preoptic and postoptic areas but not in the brainstem. Our results suggest that the presence of neurons with a dopaminergic/glutamatergic co-phenotype is a primitive character shared by jawless and jawed vertebrates. However, important differences in the distribution of these neurons and fibres were noted among the few vertebrates investigated to date. This study offers an anatomical basis for further work on the role of glutamate in dopaminergic neurons.

Individual Dopaminergic Neurons of Lamprey SNc/VTA Project to Both the Striatum and Optic Tectum but Restrict Co-release of Glutamate to Striatum Only

“…Although several factors can affect this estimation (e.g., detection method and threshold), the lamprey SNc/VTA shows a high vGluT-to-TH ratio and a high co-expression of vGluT and dopamine (Figures 1F and 1G; Table 1). Previous studies did not find co-localization of dopamine and glutamate or GABA [26,27], most likely due to low sensitivity of the used methods. However, a recent study indicated co-expression of glutamate and dopamine in lamprey SNc/VTA neurons [28].…”

“…We next examined whether TH/vGluT-immunopositive terminals from the SNc/VTA are present in the striatum and tectum. Tracer injections into the SNc/VTA ( Figure 3A) combined with immunohistochemistry for vGluT and TH showed that many TH/vGluT fibers originating from the SNc/VTA are present in the striatum (see also [26]; Figure 3B, arrowheads; N = 3). These results suggest that, as in mammals [7], dopamine and glutamate may be co-released in the striatum.…”

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

“…Here, the possibility that dopamine (DA) could modulate olfactory processing taking place in the medOB was examined. Dopaminergic processes and cells were previously observed in the OB of lampreys (Barreiro‐Iglesias, Villar‐Cervino, Anadon, & Rodicio, ; Fernandez‐Lopez, Sobrido‐Camean, Anadon, Rodicio, & Barreiro‐Iglesias, ; Pierre, Mahouche, Suderevskaya, Reperant, & Ward, ; Pierre, Rio, Mahouche, & Repérant, ; Pombal, El Manira, & Grillner, ), as in every other vertebrate studied (Smeets & Gonzalez, ). Also, cells expressing D1 or D2 receptors have been observed in the OB (Pérez‐Fernández, ; Pérez‐Fernández et al, ).…”

Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus

“…For the nomenclature of brain regions and brain nuclei we followed the nomenclature used by our group in recent studies on the organization of different neuronal systems (including neuropeptidergic systems) in the sea lamprey brain (Barreiro-Iglesias et al, 2017; Fernández-López et al, 2017). In some instances, equivalencies to nomenclatures used by other authors are mentioned in the results and discussion.…”