Octopamine is the synaptic transmitter between identified neurons in the buccal feeding network of the pond snail Lymnaea stagnalis

We report the pharmacological properties of synaptic connections from the three octopamine-containing OC interneurons to identified buccal feeding neurons in the pond snail, Lymnaea stagnalis. Intracellular stimulation of an OC interneuron evokes inhibitory postsynaptic potentials in the B3 motoneurons and N2 (d) interneurons, while the synapse between OC and N3 (phasic) interneurons has two components: an initial electrical excitation followed by chemical inhibition. All synaptic responses persist in a saline with elevated calcium and magnesium suggesting that the connections are monosynaptic. Local perfusion of 10(-4) M octopamine products the same inhibitory membrane responses from these buccal neurons as OC stimulation. These responses also persist in high Mg2+/Ca2+ saline indicating direct membrane effects. The similarities in reversal potentials for the synaptic hyperpolarization evoked on B3 neurons after OC stimulation (-89.0 mV. S.E.M.=14.1, n=10) and the octopamine response of the B3 neurons (-84.7 mV, S.E.M.=6.6. n=6) indicate that increased K+-conductance underlies both responses. Bath application of the octopaminergic drugs phentolamine (10(-6) M), epinastine (10(-6) M) or DCDM (10(-4) M) blocks the inhibitory synapse onto B3 or N2 neurons and the chemical component of the N3 response. They also block the octopamine-evoked inhibition of B3. N2 and N3 neurons. NC-7 (2x10(-5) M) has a hyperpolarizing agonist effect (like octopamine) on these neurons and also blocks their chemical synaptic input from the OC interneurons. These results provide pharmacological evidence that the neurotransmitter between the octopamine-immunopositive OC interneurons and its followers is octopamine. This is the first example of identified octopaminergic synaptic connections within the snail CNS. (C) 2000 Elsevier Science B.V. All rights reserved.