Peptidergic modulation of patterned motor activity in identified neurons of Helisoma

Abstract

The neuroaftive peptides SCPB (small cardioactive peptide B) and FMRFamide (Phe-Met-Arg-Phe-NH2), both originally isolated from molluscs, have potent modulatory effects upon the production of patterned motor activity in identified neurons (e.g., B5 and B19) in the buccal ganglia of the snail Helisoma. Such patterned motor activity has previously been shown to underlie feeding behavior. (7,8).Several aspects of the neural basis of feeding in the snail Helisoma trivolvis have been described. Cyclical activity of many identified effector neurons and elements of the central pattern generator has been characterized (9-11). In addition, the monoamines serotonin (12) and dopamine (13) have been shown to activate or modulate such patterned motor activity (PMA) associated with feeding and generated by neurons in the buccal ganglia. As a first step in characterizing the potential roles of neuroactive peptides in regulating feeding behavior in Helisoma, we report here that two neuroactive peptides, originally discovered in molluscs, have profound effects on the production of PMA (which apparently represents "fictive feeding") by buccal ganglion neurons. Small cardioactive peptide B (SCPB, Met-Asn-Tyr-Leu-Ala-PhePro-Arg-Met-NH2; ref. 14) has stimulatory effects upon the generation of PMA that resemble, at least superficially, those described for serotonin (5-hydroxytryptamine) and dopamine. In contrast, FMRFamide (Phe-Met-Arg-Phe-NH2; ref.15) inhibits and, at a sufficient concentration (10-5 M), effectively suppresses PMA in the buccal ganglia. SCP has been indicated, by chromatographic techniques, to occur in Helisoma central nervous system (see table 1 in ref. 14). We show here that the buccal ganglion ofHelisoma contains both neurons with SCPB-like immunoreactivity and neurons with anti-FMRFamide immunoreactivity.MATERIALS AND METHODS Albino specimens of Helisoma trivolvis were used; they were obtained from stocks maintained in the laboratory of A. G. M. Bulloch (University of Calgary) and derived from the Oregon Red stock of S. B. Kater's laboratory (University of Iowa). The dissection, the physiological saline, and the electrophysiological recording and display techniques have been described (16,17). For these experiments, either isolated buccal ganglia or buccal ganglia attached to the central ring of ganglia via the cerebrobuccal connectives were used. There was no detectable difference in the effects of peptides upon PMA whether or not the central ganglia were attached, but the rate of spontaneous PMA varies considerably and tends to be higher in isolated buccal ganglia. Once it had been determined that SCPB was excitatory and FMRFamide was inhibitory, relatively quiescent preparations were used for SCPB experiments and relatively active preparations were used for FMRFamide experiments. The synthetic peptides, SCPB (Peninsula Laboratories, San Carlos, CA) and FMRFamide (Sigma), were used. Saline volume (<0.5 ml) in the recording chamber was maintained by suction from the surface, and solutions were changed ...

Neural network controlling feeding in Lymnaea stagnalis: Immunocytochemical localization of myomodulin, small cardioactive peptide, buccalin, and FMRFamide‐ related peptides

“…The use of a SEEPLY-antiserum revealed a unique immunoreactive pair of cells within the buccal ganglia with axonal projections into the laterobuccal nerve, innervating the buccal mass. Thus it appears that Lymnaea differs from Helisoma and Aplysia where several FMRFamide-immunoreactive pairs of cells were detected in the buccal ganglia (Murphy et al, 1985;Church and Lloyd, 1991).…”

Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

“…Buccal peptidegic neurons innervating the foregut similar to that described here for Bc-FG cells were identified in several gastropod species: Aplysia , B2 in Lymnaea (Perry et al, 1998), B5 in Helisoma (Murphy and Kater, 1980;Murphy et al, 1985) and B11/B12 in Tritonia (Lloyd and Willows, 1988). All these cells have a similar morphology: a large cell body and main neurite leaving the CNS through the gastro-esophageal nerve and innervating the foregut.…”

Peptidergic motoneurons in the buccal ganglia of Aplysia californica Immunocytochemical, morphological, and physiological characterizations

“…Previous studies have shown a wide variety of central actions of SCPs in Aplysia (Abrams et al 1984;Ocorr and Byrne 1986;Sossin et al 1987;Alevizos et al 1989;Kirk 1989;Plummer and Kirk 1990;Taussig et al 1989), as well as in Limax (Prior and Watson 1988;Hess and Prior 1989), Tritonia (Lloyd and Willows 1980;Willows et al 1988), and Helisoma (Murphy et al 1985). For example, in the abdominal ganglia of Aplysia, the R20 neurons modulate respiratory pumping by exciting the cells of the R25/L25 network.…”