Peptide B induction of bag‐cell activity in Aplysia: Localization of sites of action to the cerebral and pleural ganglia

Abstract

The bag cells of the marine mollusc Aplysia are model neuroendocrine cells involved in the initiation of egg laying and its associated behaviors, but the natural stimulus triggering bag-cell activity is not known. The atrial gland of A. californica, an exocrine organ in the reproductive tract, contains two structurally related peptides (A and B) which can induce an afterdischarge in vitro, and these peptides can be used to probe the central nervous system for sites where extrinsic excitatory input onto the bag-cell system might occur. These sites were identified in a series of lesion and ablation experiments. The entire central nervous system was removed from an animal and placed in a chamber with two compartments which could be independently perfused, allowing peptides (atrial gland extract or purified peptide B) to be selectively applied to specific regions of the nervous system while bag-cell activity was monitored using extracellular suction electrodes. Afterdischarges were consistently and reliably induced when peptides were applied to the cerebral ganglion, the pleural ganglia, the cerebropleural connectives, or the rostral 10-15% of the pleurovisceral connectives, provided that an intact neuronal pathway connected the site of peptide application with the bag cells. In contrast, afterdischarges were never observed when peptides were selectively applied to the buccal or pedal ganglia and only rarely observed when applied to the abdominal ganglion and caudal pleurovisceral connectives. These results support the hypothesis that bag-cell processes and/or neuron(s) presynaptically excitatory to the bag cells are located in the pleural and cerebral ganglia and narrow the region of the central nervous system where the critical initiator element(s) can be identified.

Complex behavior induced by egg-laying hormone in Aplysia

“…We injected a second group of animals with homogenized atrial gland. Peptides that are present in the atrial gland in high amounts have been shown to trigger a burst discharge of the bag cells (Painter et al 1988). The gland also contains three other ELHlike peptides, the califins, which mimic the action of ELH when applied to central neurons ).…”

The Roles of Transcription and Translation in Mediating the Effect of Electrical Afterdischarge on Neurohormone Synthesis inAplysiaBag Cell Neurons1

“…In in vivo experiments, animals (n ϭ 4 -5/group) were injected with atrial gland peptides A and B (1-2 g/g BW; see below). These peptides activate cells in the cerebral and pleural ganglia that, in turn, transmit neural signals to the bag cells in the abdominal ganglia to stimulate an afterdischarge (19). Egg-laying and its related behaviors induced by peptides A and B were observed.…”

Nitric oxide induces aspects of egg-laying behavior in Aplysia

“…Thus, neurons in the cerebral and pleural ganglia containing peptides of the bag cells family apparently function in egg laying Painter et al, 1988;Pulst et al, 1988). In addition, peptides related to those expressed in identified neuron R15 are also expressed in other neurons active in autonomic control (Romanova et al, 2007).…”

“…The bag cells are generally silent, except preceding egg laying (Dudek et al, 1979;Pinsker and Dudek, 1977). Electrical or chemical stimulation of cerebral and pleural ganglion neurons can trigger a bag cell discharge Painter et al, 1988). Brief electrical stimulation of the pleural-abdominal connectives also initiates a bag cells discharge (Ferguson et al, 1989a;Kupfermann and Kandel, 1970;Pinsker and Dudek, 1977;Wayne and Wong, 1994), presumably because the stimulus excites axons from the head ganglia that activate the bag cells.…”

“…The peptides are synthesized on a single precursor protein, which is then cleaved (Nagle et al, 1989;Scheller et al, 1983). Homologues of the bag-cell peptides are also synthesized in and released from the atrial gland of the genital tract Heller et al, 1980;Nagle et al, 1989;Painter et al, 1988;Scheller et al, 1982). In some Aplysia species, including in A. fasciata that was used in this study, a distinct atrial gland is not present, and tissue homologous to the atrial gland is present in the anterior portion of the large hermaphroditic duct (Painter et al, 1985).…”