Food avoidance learning is accompanied by synaptic attenuation in identified interneurons controlling feeding...

Identified paracerebral feeding command interneurons (PCNs) in the brain of the mollusc Pleurobranchaea excite other identified PCNs by means of a chemical polysynaptic pathway whose efficacy is reduced by food avoidance training (conditionally paired food and electric shock). The purpose of the present study was to identify the neurons comprising this pathway and to localize learning-induced changes to single identified neurons. We found that associative training strongly attenuates or abolishes a unitary excitatory postsynaptic potential (EPSP) at a single identified synapse in this polysynaptic pathway, but does not alter other synapses. The PCNs descend to the buccal ganglion, where they monosynaptically excite each member of a set of four identified neurons (two per hemiganglion) that belong to the corollary discharge population described previously. The strength of ascending and descending synapses involving identified PCNs is greatest ipsilaterally and is proportional to relative command efficacy established in previous studies. These findings suggest that command efficacy results directly from synaptic strength. The pair of corollary discharge neurons on each side of the buccal ganglion sends axons to the opposite side and thence up the contralateral cerebrobuccal connective to the brain. These neurons have therefore been termed the contralateral corollary discharge (CCD) neurons. Each CCD monosynaptically excites every PCN on both sides of the brain. Contralateral synaptic influences on identified PCNs are larger than ipsilateral ones. Each of the four identified CCD neurons is electrically coupled to all other members of the subset, including the contralateral homologue (based on simultaneous intracellular recording) and the ipsilateral partner (based on dye coupling). Hyperpolarizing a single CCD eliminates the polysynaptic response of PCNs to stimulation of other PCNs, whereas depolarizing a single CCD mimics the polysynaptic response. The CCD neurons are therefore necessary and sufficient to the polysynaptic response. Consistent with this role, the CCDs discharge in phase with the PCNs during the feeding motor program, and hyperpolarizing a CCD abolishes the cycle discharge of PCNs and weakens the feeding rhythm. Of the several reciprocal synapses identified between the PCNs and CCDs, only one was significantly altered by associative training in the food avoidance paradigm developed previously. This synapse, from the polysynaptic excitor (PSE) to the ipsilateral CCD, was also the strongest in this recurrent positive-feedback loop. In brains taken from conditioned specimens, the mean EPSP amplitude induced by a PSE action potential in ipsi