Second messengers of octopamine receptors in the snail Lymnaea.

We describe octopamine responses of 3 large buccal neurons of Lymnaea and test the hypothesis that these are cAMP-dependent. The B1 neuron is excited by octopamine and the depolarisation is significantly enlarged (P < 0.05) by application of the blocker of cAMP breakdown, 3-isobutyl-1-methylxanthine (IBMX). The B1 neuron is also depolarised by forskolin, an activator of adenylyl cyclase. The B2 and B3 neurons are inhibited by octopamine, and the response is not affected by IBMX. Both cells are excited by forskolin. We conclude that the B1 neuron response to octopamine is likely to be mediated by cAMP, while the B2 and B3 responses are cAMP-independent.

Octopaminergic modulation of the membrane currents in the central feeding system of the pond snail Lymnaea stagnalis.

Octopamine is released by the intrinsic OC interneurons in the paired buccal ganglia and serves both as a neurotransmitter and a neuromodulator in the central feeding network of the pond snail Lymnaea stagnalis. The identified B1 buccal motoneuron receives excitatory inputs from the OC interneurons and is more excitable in the presence of 10 microM octopamine in the bath. This modulatory effect of octopamine on the B1 motoneuron was studied using the two electrode voltage clamp method. In normal physiological saline depolarising voltage steps from the holding potential of -80 mV evoke a transient inward current, presumably carried by Na(+) ions. The peak values of this inward current are increased in the presence of 10 microM octopamine in the bath. In contrast, both the transient (IA) and delayed (IK) outward currents are unaffected by octopamine application. Replacing the normal saline with a Na(+)-free bathing solution containing K(+) channel blockers (50 mM TEACl, 4 mM 4AP) revealed the presence of an additional inward current of the B1 neurons, carried by Ca(2+). Octopamine (10 microM) in the bath decreased the amplitudes of this current. These results suggest that the membrane mechanisms which underlie the modulatory effect of octopamine on the B1 motoneuron include selective changes of the Na(+)- and Ca(2+)-channels.

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

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.

Heterosynaptic modulation by the octopaminergic OC interneurons increases the synaptic outputs of protraction phase interneurons (SO, N1L) in the feeding system of Lymnaea stagnalis.

We examined the cholinergic synapses between protraction phase interneurons (SO or N1L) and their targets (N1M interneuron, B1 motoneuron) in the buccal ganglia of the pond snail Lymnaea stagnalis. We have tested the hypothesis that the OC (octopamine-containing) interneuron, an intrinsic modulator of the feeding network, can increase the synaptic efficacy from the SO or N1L to their targets. Prestimulation of the OC interneuron, 4 s before the activation of the SO or N1L increases the strength of their output synapses by 75% (SO)-110% (N1L). The individual excitatory postsynaptic potentials evoked by SO or N1L stimulation increase in size. OC prestimulation also produces an increase in the firing rate of these presynaptic interneurons: SO 40%; N1L 33%. The facilitation lasts up to 6 s after the end of the OC burst. The enhancement of PSPs is seen at all the output synapses (both excitatory and inhibitory) of the SO and N1L interneurons. The output synapses of the non-cholinergic swallowing phase N3p interneuron are not affected, even when the same postsynaptic target is selected. The SO-->N1M, SO-->B1 and N1L-->N1M synapses are also strengthened by bath application of 1-5 microM octopamine (average increase 60%). The major effect is an increased excitability of the SO; the B1 motoneuron response to the main transmitter of the SO, acetylcholine, is unaffected. Increased synaptic outputs of the protraction phase SO and N1L interneurons is functionally significant for generation of feeding pattern in the Lymnaea CNS. Strengthening the connections of SO and N1L to the central pattern generator (N1M) interneurons enhances their ability to drive fictive feeding. Thus heterosynaptic facilitation by the octopaminergic OC interneurons in the central pattern generator network may contribute to the behavioral plasticity of feeding in the intact animal.

Comparative neuroethology of feeding control in molluscs.

Over the last 30 years, many laboratories have examined, in parallel, the feeding behaviour of gastropod molluscs and the properties of the nervous system that give rise to this behaviour. Equal attention to both behavioural and neurobiological issues has provided deep insight into the functioning of the nervous system in generating and controlling behaviour. The conclusions derived from studies on gastropod feeding are generally consistent with those from other systems, but often provide more detailed information on the behavioural function of a particular property of the nervous system. A review of the literature on gastropod feeding illustrates a number of important messages. (i) Many of the herbivorous gastropods display similarities in behaviour that are reflected in corresponding similarities in neural anatomy, pharmacology and physiology. By contrast, the same aspects of the behaviour of different carnivorous species are quite variable, possibly because of their specialised prey-capture techniques. Nonetheless, some aspects of the neural control of feeding are preserved. (ii) Feeding in all species is flexible, with the behaviour and the physiology adapting to changes in the current environment and internal state and as a result of past experience. Flexibility arises via processes that may take place at many neural sites, and much of the modulation underlying behavioural flexibility is understood at a systems and at a cellular level. (iii) Neurones seem to have specific functions that are consistent with their endogenous properties and their synaptic connections, suggesting that individual neurones code specific pieces of information (i.e. they are 'grandmother cells'). However, the properties of a neurone can be extremely complex and can be understood only in the context of the complete neural circuit and the behaviour that it controls. In systems that are orders of magnitude more complex, it would be impossible to understand the functional properties of an individual neurone, even if it also coded specific information. (iv) Systems such as gastropod feeding may provide a model for understanding the functional properties of more complex systems.