Immunocytochemical localization of dopamine and its synthetic enzymes in the central nervous system of the lampreyLampetra fluviatilis

Abstract

The distribution of dopamine (DA)-containing cell bodies, fibers, and terminals in the brain and spinal cord of Lampetra fluviatilis was investigated by immunohistochemical means. In order to distinguish dopaminergic neurons from those using other catecholamines as the primary neurotransmitter, the distribution of dopamine-immunoreactive structures was compared to that of cell bodies, fibers, and terminals labelled with antibodies directed against the enzymes tyrosine hydroxylase (TH), aromatic L-amino acid decarboxylase (AADC), dopamine beta-hydroxylase (DBH), and phenylethanolamine-N-methyl transferase (PNMT). We define dopaminergic neurons as those that are simultaneously DA, TH, and AADC immunoreactive and at the same time DBH and PNMT nonreactive. The overall concentrations of dopamine, noradrenaline, and adrenaline and some of their metabolites were also measured via high-performance liquid chromatography of whole-brain extracts. Our results revealed the presence of 10 populations of dopaminergic neurons in the brain of the lamprey in the olfactory bulb, preoptic area, hypothalamus, rhombencephalon, and spinal cord. In addition, uniquely DA-immunoreactive neurons, in contact with the cerebrospinal fluid, were observed in the hypothalamus and spinal cord. Chromatography indicated that dopamine exists in considerably higher concentrations than noradrenaline in the lamprey brain, whereas adrenaline is absent, the latter finding being supported by our failure to observe any PNMT-immunoreactive cell bodies, fibers, or terminals. The dopaminergic system of the lamprey appears to share many features not only with that of other anamniotes but also with that of amniotes; however, as in teleosts, dopaminergic neurons in the midbrain corresponding to the substantia nigra, the retrorubral area, and the ventral tegmental area of other species do not exist in the lamprey.

The Dopamine D2 Receptor Gene in Lamprey, Its Expression in the Striatum and Cellular Effects of D2 Receptor Activation

“…The general distribution pattern of dopamine-immunoreactive neurons in this nucleus is similar to that obtained using antibodies against aromatic L-amino acid decarboxylase or TH [9], [30], [42] and furthermore this nucleus does not express the enzymes involved in the synthesis of noradrenaline or adrenaline [42] implying that the neurons are dopaminergic.…”

Expression of a Novel D4 Dopamine Receptor in the Lamprey Brain. Evolutionary Considerations about Dopamine Receptors

“…The lamprey dopamine expression pattern ( Pierre et al, 1994 , 1997 ; Pombal et al, 1997 ; Pierre-Simons et al, 2002 ; Abalo et al, 2005 ) is quite similar to that reported in other vertebrates. It has recently been shown that dopamine has a conservative role in modulating the excitability of D1 and D2 receptor expressing striatal neurons of the direct and indirect pathways ( Robertson et al, 2012 ; Ericsson et al, 2013 ).…”

“…Dopamine acts through two evolutionarily convergent classes of G-protein-coupled receptors (GPCRs), D1 and D2 ( Kebabian and Calne, 1979 ; Beaulieu and Gainetdinov, 2011 ). In the last decades, several reports suggest that the dopaminergic system is highly conserved in vertebrates, according to the data reported in lampreys ( Pierre et al, 1994 , 1997 ; Pombal et al, 1997 ; Pierre-Simons et al, 2002 ; Abalo et al, 2005 ; Barreiro-Iglesias et al, 2010 ; Robertson et al, 2012 ; Ericsson et al, 2013 ; Pérez-Fernández et al, 2014b ). These animals, together with hagfishes, represent the oldest living branch of vertebrates that diverged from the main branch leading to vertebrates around 560 million years ago ( Kumar and Hedges, 1998 ).…”

A Novel Neural Substrate for the Transformation of Olfactory Inputs into Motor Output

“…Synaptic responses in RS neurons were observed only when this medial OB region was stimulated, and axons projected prominently from this site to the PT—a region with abundant dopaminergic neurons, and proposed by some to be equivalent to the ventral tegmental area of mammals [39]. We have shown that this olfactory-locomotor transformation also involves the MLR, a region with a central role in initiating and controlling locomotion [18],[19],[40].…”