Neuromeric Distribution of Nicotinamide Adenine Dinucleotide Phosphate-Diaphorase Activity in the Adult Lamprey Brain.

Manuel A Pombal,Daniel Lozano,Jesús M López,Manuel Megías

doi:10.3389/fnana.2022.826087

Abstract

This study reports for the first time the distribution and morphological characterization of nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d; a reliable marker of nitric oxide synthase activity) positive elements in the central nervous system of the adult river lamprey (Lampetra fluviatilis) on the framework of the neuromeric model and compares their cytoarchitectonic organization with that of gnathostomes. Both NADPH-d exhibiting cells and fibers were observed in all major divisions of the lamprey brain as well as in the spinal cord. In the secondary prosencephalon, NADPH-d positive cells were observed in the mitral cell layer of the olfactory bulb, evaginated pallium, amygdala, dorsal striatum, septum, lateral preoptic nucleus, caudal paraventricular area, posterior entopeduncular nucleus, nucleus of the stria medullaris, hypothalamic periventricular organ and mamillary region sensu lato. In the lamprey diencephalon, NADPH-d labeled cells were observed in several nuclei of the prethalamus, epithalamus, pretectum, and the basal plate. Especially remarkable was the staining observed in the right habenula and several pretectal nuclei. NADPH-d positive cells were also observed in the following mesencephalic areas: optic tectum (two populations), torus semicircularis, nucleus M5 of Schöber, and a ventral tegmental periventricular nucleus. Five different cell populations were observed in the isthmic region, whereas the large sensory dorsal cells, some cells located in the interpeduncular nucleus, the motor nuclei of most cranial nerves, the solitary tract nucleus, some cells of the reticular nuclei, and small cerebrospinal fluid-contacting (CSF-c) cells were the most evident stained cells of the rhombencephalon proper. Finally, several NADPH-d positive cells were observed in the rostral part of the spinal cord, including the large sensory dorsal cells, numerous CSF-c cells, and some dorsal and lateral interneurons. NADPH-d positive fibers were observed in the olfactory pathways (primary olfactory fibers and stria medullaris), the fasciculus retroflexus, and the dorsal column tract. Our results on the distribution of NADPH-d positive elements in the brain of the adult lamprey L. fluviatilis are significantly different from those previously reported in larval lampreys and demonstrated that these animals possess a complex nitrergic system readily comparable to those of other vertebrates, although important specific differences also exist.

Highlights

Reduced nicotinamide adenine dinucleotide phosphatediaphorase (NADPH-d) histochemistry has been extensively used for detection of specific cell populations in both the central (CNS) and peripheral nervous systems
Most of the NADPH-d labeled cell populations detected in the lamprey CNS were located in the forebrain and midbrain, but some NADPH-d positive cells were identified in the hindbrain, and in the rostral spinal cord
Apart from the description of the complex nitrergic system, the technique used in our study was confirmed as a powerful tool for the identification of cell groups and brain structures that are otherwise indistinct in the lamprey brain

Summary

Introduction

Reduced nicotinamide adenine dinucleotide phosphatediaphorase (NADPH-d) histochemistry has been extensively used for detection of specific cell populations in both the central (CNS) and peripheral nervous systems (see Alonso et al, 2000). The histochemical staining for NADPH-d was identified to be associated with nitric oxide synthase (NOS; Bredt et al, 1991a; Dawson et al, 1991; Hope et al, 1991). NOS is the enzyme that catalyzes the synthesis of nitric oxide, a gaseous messenger molecule (Bredt and Snyder, 1992), from L-arginine. There are different types of NOS: neuronal NOS (nNOS) and endothelial NOS (eNOS), which are constitutively expressed in the nervous system, and induced NOS (iNOS) in the macrophages. In the CNS of anamniotes (excluding amphibians), NO is mainly produced by nNOS, whereas eNOS, together with nNOS, contributes to produce NO in amphibians and amniotes (reviewed in Toda and Ayajiki, 2006)

Results

Discussion

Conclusion