Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc Lymnaea stagnalis

Abstract

The pleural interneuron PlB is a white neuron in the pleural ganglion of the snail Lymnaea. We test the hypothesis that it inhibits neurons at all levels of the feeding system, using a combination of anatomy, physiology and pharmacology. There is just one PlB in each pleural ganglion. Its axon traverses the pedal and cerebral ganglia, running into the buccal ganglia. It has neuropilar branches in the regions of the cerebral and buccal ganglia where neurons that are active during feeding also branch. Activation of the PlB blocks fictive feeding, whether the feeding rhythm occurs spontaneously or is driven by a modulatory interneuron. The PlB inhibits all the neurons in the feeding network, including protraction and retraction motoneurons, central pattern generator interneurons, buccal modulatory interneurons (SO, OC), and cerebral modulatory interneurons (CV1, CGC). Only the CV1 interneuron shows discrete 1:1 IPSPs; all other effects are slow, smooth hyperpolarizations. All connections persist in Ca(2+)/Mg(2+)-rich saline, which reduces polysynaptic effects. The inhibitory effects are mimicked by 0.5 to 100 micromol l(-1) FMRFamide, which the PlB soma contains. We conclude that the PlB inhibits neurons in the feeding system at all levels, probably acting though the peptide transmitter FMRFamide.

The role of RFamide peptides in feeding

“…Feeding-induced arousal and food intake in snails are regulated to a large extent by serotonergic 5-hydroxytryptamine (5-HT) and dopaminergic neurons (Murphy 2001, Elliott & Susswein 2002. FMRFamide and FMRFamide-containing pleural neurons both inhibit feeding and facilitate withdrawal behaviour in various gastropod species (Kyriakides & McCrohan 1989, Murphy 1990, Alania et al 2004. This is achieved by FMRFamide rapidly attenuating the rhythmic firing of buccal and cerebral ganglion neurons responsible for initiating and maintaining the repetitive motor outputs required for feeding (Alania et al 2004).…”

“…FMRFamide and FMRFamide-containing pleural neurons both inhibit feeding and facilitate withdrawal behaviour in various gastropod species (Kyriakides & McCrohan 1989, Murphy 1990, Alania et al 2004. This is achieved by FMRFamide rapidly attenuating the rhythmic firing of buccal and cerebral ganglion neurons responsible for initiating and maintaining the repetitive motor outputs required for feeding (Alania et al 2004). In addition, FMRFamide acts directly on muscle groups, such as the pharyngeal retractor muscle (PRM) to antagonise 5-HT signalling and strengthen and prolong contraction (which facilitates withdrawal; Hernadi et al 2005).…”

Neuroanatomical, immunocytochemical, and physiological studies of the pharyngeal retractor muscle and its putative regulatory neurons playing a role in withdrawal and feeding in the snail, Helix pomatia

“…Both FMRFa and pleural FMRFacontaining interneurons are able to suppress the activity of the buccal feeding CPG and additionally facilitate withdrawal responses in various gastropod species including Helix (Alania and Sakharov 2000; for a review, see Alania et al 2004). We have found that the identified pedal LP3 5-HTergic PRM neuron ) also contains FMRFa, supplying the PRM with both 5-HT and FMRFa.…”

“…When escaping, whole body withdrawal suppresses any other behavior including feeding (Davis et al 1974(Davis et al , 1977Alania et al 2004), suggesting that the activity of withdrawal and feeding networks can suppress the activity of each other. Both FMRFa and pleural FMRFacontaining interneurons are able to suppress the activity of the buccal feeding CPG and additionally facilitate withdrawal responses in various gastropod species including Helix (Alania and Sakharov 2000; for a review, see Alania et al 2004).…”

“…In gastropods, the degree of satiation depends on the actual level of feeding arousal and on food intake, which is regulated by both serotonergic and dopaminergic neurons (for reviews, see Weiss et al 1981;Elliott and Susswein 2002;Murphy 2001), suggesting that both seratonin (5HT) and dopamine (DA) neurons play an important role in the regulation of withdrawal behavior and CM contraction. In contrast, the neuropeptide FMRFamide (FMRFa) and the FMRFa-containing pleural neurons stop the feeding program and facilitate withdrawal behavior in Lymnaea (Kyriakides and McCrohan 1989;Alania et al 2004), Helisoma (Murphy et al 1985;Murphy 1990), and Limax (Cooke and Gelperin 1988), indicating that FMRFa-containing neurons play an important role in the regulation of the withdrawal reaction. Since the PRM is involved in both withdrawal and feeding behaviors, which are largely exclusive, we propose that 5HT, DA, and FMRFa are also involved in the regulation of both phasic and sustained contractions of the PRM during feeding and withdrawal.…”