Long-lasting reconfiguration of two interacting networks by a cooperation of presynaptic and postsynaptic plasticity

The functional reconfiguration of central neuronal networks, a phenomenon by which neurons change their participation in network operation, is important for organizing adaptive behaviors. Such reconfiguration can be expressed in a long-lasting manner (hours, days) after a training paradigm. The present study shows that such a long-lasting network reconfiguration requires a cooperation of both presynaptic and postsynaptic modifications in a neuronal interaction between two functionally distinct networks. In isolated preparations of the lobster stomatogastric nervous system, the single ventral dilator (VD) neuron can switch its functional participation from one discrete network (the pyloric network) to another (the cardiac sac network). This switching capability can be long-lasting and can be induced by a sensitizing procedure. A persistent change that was associated with this neuronal switching was found in each of the two networks. First, the intrinsic membrane properties of the VD neuron that allow it to participate spontaneously in the pyloric network are altered. Second, bursting activity is strengthened in the inferior ventricular neurons that both drive cardiac sac network activity and monosynaptically excite the VD neuron in phase with this network activity. Importantly, these changes in intrinsic properties of both presynaptic and postsynaptic neurons are required to allow the VD neuron switching, because expression of either the presynaptic or the postsynaptic change alone did not permit VD neuron switching to occur. These results suggest that a cooperative modification of a discrete network interaction is able to persistently switch the output pattern of a motor neuron as a result of a sensitizing paradigm.