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Compartmentalization of Information Processing in anAplysia Feeding Circuit Interneuron through Membrane Properties and Synaptic Interactions

We describe a pair of cerebral-to-buccal interneurons, CBI-5/6, which have outputs and inputs in two ganglia. The soma in the cerebral ganglion received synaptic inputs during buccal motor programs (BMPs) and after mechanical stimulation of the lips. During BMPs the soma received antidromic spikes generated in processes in the buccal ganglion. The soma was driven into a plateau potential by each of these inputs, during which it fired orthodromically at 0–5 Hz. The soma had outputs in the cerebral ganglion consisting of electrical coupling to the adjacent CBI-5/6 and to a cerebral-to-pedal neuron (CPN1). The buccal terminals of CBI-5/6 received inputs that generated rhythmic barrages (up to 25 Hz) of antidromic spikes during BMPs. The buccal terminals had chemical and electrical outputs to motor and premotor elements of feeding circuitry. This combination of synaptic interactions and endogenous properties mean that CBI-5/6 can process information in a number of ways. During the barrage of antidromic spikes, high-frequency firing will produce strong inputs to buccal followers and on their arrival at the soma will transfer excitation electrotonically to CPN1. Subthreshold input to the soma will be transferred electrotonically to cerebral followers but will not be relayed to postsynaptic buccal neurons. Plateau potentials after the antidromic spikes or local cerebral inputs will locally excite CPN1 via electrical coupling but will have little influence on buccal events because of the low orthodromic firing rate. Thus, CBI-5/6 may transmit information locally within the cerebral ganglion or more extensively in both buccal and cerebral ganglia simultaneously.