Cellular and synaptic mechanisms responsible for a long-lasting restructuring of the lobster pyloric network

1. In the lobster Palinurus vulgaris a sensory input in the lateral posterolateral nerve (lpln) of the stomatogastric nervous system (STS) is able to turn on the cardiac sac (CS) network and to induce dramatic long-lasting alterations in the output of the pyloric network. This long-lasting alteration of pyloric network output consists primarily of changes in the activity of the two neurons that innervate the muscles of the cardiopyloric valve of the stomach, with the dilator neuron (the ventricular dilator, VD) transferring from the pyloric network to the CS network and the constrictor neuron (the inferior cardiac, IC) shifting to fire earlier in the pyloric pattern. 2. The inferior ventricular (IV) neurons of the CS network make complex multiaction synaptic connections onto several pyloric neurons in a related species, Panulirus interruptus. We show that many of the short-term alterations in pyloric activity observed during CS network bursts in Palinurus are due to similar IV neuron synaptic connections. However, the long-lasting effects of lpln stimulation on pyloric output are not due to this synaptic input, because 1) direct activation of the IV neurons does not induce long-lasting changes in pyloric activity and 2) pharmacologic disconnection of this synaptic input does not abolish lpln stimulation's long-lasting effects. Lpln stimulation therefore activates two different neuronal inputs to the pyloric network. 3. The transfer of the VD neuron from the pyloric to the CS network is the result of the concerted actions of these two inputs. Lpln stimulation turns on the CS network, and the IV neurons of the CS network excite the VD neuron and ensure it fires with the CS network. The second neuronal input (that not involving known CS network neurons) abolishes in a long-lasting fashion the VD neuron regenerative (plateau) properties, and thus suppresses the ability of the VD neuron to participate in the pyloric rhythmic pattern between CS network bursts. 4. Experimental manipulation of VD neuron activity can both mimic and reverse the effects of lpln stimulation on the IC neuron. The changes in IC neuron activity are therefore not due to direct lpln-activated synaptic input onto the IC neuron, but instead are indirect "network" effects arising from the changes in VD neuron activity.