Histamine and gamma-aminobutyric acid in the nervous system of Pygospio elegans (Annelida: Spionidae): structure and recovery during reparative regeneration

Abstract

Background In recent two decades, studies of the annelid nervous systems were revolutionized by modern cell labeling techniques and state-of-the-art microscopy techniques. However, there are still huge gaps in our knowledge on the organization and functioning of their nervous system. Most of the recent studies have focused on the distribution of serotonin and FMRFamide, while the data about many other basic neurotransmitters such as histamine (HA) and gamma-aminobutyric acid (GABA) are scarce. Results Using immunohistochemistry and confocal microscopy we studied the distribution of histamine and gamma-aminobutyric acid in the nervous system of a spionid annelid Pygospio elegans and traced their redevelopment during reparative regeneration. Both neurotransmitters show specific patterns in central and peripheral nervous systems. HA-positive cells are concentrated mostly in the brain, while GABA-positive cell somata contribute equally to brain and segmental ganglia. Some immunoreactive elements were found in peripheral nerves. Both substances were revealed in high numbers in bipolar sensory cells in the palps. The first signs of regenerating HAergic and GABAergic systems were detected only by 3 days after the amputation. Further redevelopment of GABAergic system proceeds faster than that of HAergic one. Conclusions Comparisons with other annelids and mollusks examined in this respect revealed a number of general similarities in distribution patterns of HAergic and GABAergic cells in different species. Overall, the differences in the full redevelopment of various neurotransmitters correlate with neuronal development during embryogenesis. Our results highlight the importance of investigating the distribution of different neurotransmitters in comparative morphological and developmental studies.

Exploring Octopamine: Immunohistochemical research of a spionid worm <em>Pygospio elegans</em> nervous system

“…All the identified OA-like immunoreactive elements related to the peripheral nervous system are located in the palps, peristomium, gills, and body segments, and are unique in that no other neurotransmitters have been found in them (Starunova, Shunkina, Novikova, and Starunov, 2022;Barmasova, Starunova, Novikova, and Starunov, 2022). Remarkable OA-like immunopositive cells within P. elegans palps are densely arranged in rows spanning the entire length (Figs 1, 2A).…”

“…This may be due to both differences between groups and differences in the detection techniques used. It is worth noting that in P. elegans, another biogenic amine, histamine (HA), has somehow similar distribution in the central nervous system (Starunova, Shunkina, Novikova, and Starunov, 2022). Few HA-immunopositive cells were detected in the brain, while in the ventral nerve cord only HA-immunopositive nerve projections were found.…”

“…It was shown that the epithelium of the Lumbricus exhibits a diverse array of sensory cells with different chemical specificity in both the body wall (serotonin, dopamine, noradrenalin) and gut (GABA, enkephalin, FMRFamide) (Ehinger and Myhrberg, 1971). It is worth noting that the body wall of P. elegans showed a reduced diversity of sensory elements (Starunova, Shunkina, Novikova, and Starunov, 2022;Barmasova, Starunova, Novikova, andStarunov, 2022) compared to O. haakonmosbiensis (Zaitseva et al, 2022) and earthworms (Ehinger and Myhrberg, 1971;Csoknya et al, 1997), possibly due to the small body size of P. elegans. The reduced diversity of sensory elements in the body wall could be a potential reason for the absence of a similar plexus with other studied neurotrans-mitters (serotonin, FMRFamide, HA, GABA, CA) in P. elegans (Starunova, Shunkina, Novikova, and Starunov, 2022;Barmasova, Starunova, Novikova, and Starunov, 2022;Shunkina, Starunova, Novikova, and Starunov, 2023).…”

“…short list of species. Recently, we have performed a series of studies on the distribution of catecholamine-reactive (CA) (Barmasova, Starunova, Novikova, and Starunov, 2022), histamine-(HA) and gamma-aminobutyric acidimmunoreactive (GABA) elements of the nervous system in the spionid worm Pygospio elegans (Starunova, Shunkina, Novikova, and Starunov, 2022). The current study is a continuation of this series and is aimed to describe OAimmunopositive elements of the central and peripheral nervous systems of this animal.…”

“…Two different fixatives were used: a manufacturer suggested a mixture of a freshly prepared 4 % paraformaldehyde and 0.3 % glutaraldehyde in 0.1M phosphate-buffered saline (PBS) and an alternative fixative solution containing 5 ml 25 % glutaraldehyde, 15 ml saturated picric acid, and 0.2 ml glacial acetic acid (Barna et al, 2001). We used the standardized whole-mount antibody labeling method described in Starunova, Shunkina, Novikova, and Starunov, 2022. Polyclonal rabbit anti-octopamine primary antibody (Millipore, Massachusetts, USA, AB 1799, dilution 1 : 100) was used for the immunostaining process.…”