Catecholamines are believed to play an important role in regulating the properties and functional organization of the neural circuitry mediating consummatory feeding behaviors in Aplysia. In the present study, we morphologically and electrophysiologically identified a pair of catecholaminergic interneurons, referred to as B65, in the buccal ganglia. Their processes innervate both the ipsi- and contralateral neuropil, and separate branches of B65 appeared to innervate the somata of both ipsi- and contralateral B4/5 neurons. B65 exhibited patterned burst(s) of activity during spontaneous cycles of fictive feeding. Patterned activity in B65 also was elicited by stimulation of the radula nerve, by depolarization of the pattern initiating neurons B31/32 or B63, and by bath application of -3,4-dihydroxyphenylalanine (DOPA). B65 appeared to be a member of the protraction group of neurons. Action potentials in B65 elicited fast one-for-one excitatory postsynaptic potentials (EPSPs) in neurons B4/5, B8A/B, B31/32, B63, and B64. In turn, B31/32 and B63 excited B65 and B64 inhibited B65. Some of the synaptic connections of B65 were plastic. For example, the fast EPSPs elicited in B4/5 and B64 decremented, whereas those in B31/32 andB8A/B facilitated. In addition to fast EPSPs, B65 elicited slow postsynaptic potentials in some of its follower cells. Depolarization of B65 elicited cycles of patterned activity indicative of fictive feeding in buccal neurons, including B65 itself. During series of B65-induced patterns, the properties of the buccal motor programs appeared to change. In particular, the activity of radula closure motor neurons B8A/B, which initially coincided mainly with the protraction phase of a cycle, gradually extended to overlap mostly with the retraction phase. This observation suggests that prolonged activity in B65 may play a role in transitioning from rejection-like to ingestion-like fictive feeding. The phase shift of the activity of B8A/B appears due, at least in part, to a decrease in activity of B4/5, and thus a reduction in inhibition from B4/5 onto B8A/B, during the retraction phase. The functional properties and synaptic connections of B65 suggest that it may play an important role in determining features of patterned neural activity in the buccal ganglia.

The buccal ganglia of Aplysia contain a central pattern generator (CPG) that mediates rhythmic movements of the buccal apparatus during feeding. Activity in this CPG is believed to be regulated, in part, by extrinsic serotonergic inputs and by an intrinsic and extrinsic system of putative dopaminergic cells. The present study investigated the roles of dopamine (DA) and serotonin (5-HT) in regulating feeding movements of the buccal apparatus and properties of the underlying neural circuitry. Perfusing a semi-intact head preparation with DA (50 microM) or the metabolic precursor of catecholamines (L-3-4-dihydroxyphenylalanine, DOPA, 250 microM) induced feeding-like movements of the jaws and radula/odontophore. These DA-induced movements were similar to bites in intact animals. Perfusing with 5-HT (5 microM) also induced feeding-like movements, but the 5-HT-induced movements were similar to swallows. In preparations of isolated buccal ganglia, buccal motor programs (BMPs) that represented at least two different aspects of fictive feeding (i.e., ingestion and rejection) could be recorded. Bath application of DA (50 microM) increased the frequency of BMPs, in part, by increasing the number of ingestion-like BMPs. Bath application of 5-HT (5 microM) did not significantly increase the frequency of BMPs nor did it significantly increase the proportion of ingestion-like BMPs being expressed. Many of the cells and synaptic connections within the CPG appeared to be modulated by DA or 5-HT. For example, bath application of DA decreased the excitability of cells B4/5 and B34, which in turn may have contributed to the DA-induced increase in ingestion-like BMPs. In summary, bite-like movements were induced by DA in the semi-intact preparation, and neural correlates of these DA-induced effects were manifest as an increase in ingestion-like BMPs in the isolated ganglia. Swallow-like movements were induced by 5-HT in the semi-intact preparation. Neural correlates of these 5-HT-induced effects were not evident in isolated buccal ganglia, however.

Both experimental and computational approaches were used to examine how a circuit of identified neurons in the buccal ganglia of Aplysia functions as a central pattern generator (CPG) controlling aspects of feeding, the ways in which transmitters modulate the electrical activity of this circuit, and the features of consummatory behaviours that are mediated by the various patterns of electrical activity in this CPG. The biophysical properties of neurons B4, B31, B35, B51, B52 and B64, and their synaptic connections were mathematically modelled and simulated using the SNNAP computer program. In the model, brief depolarizations of B31 elicited single cycles of patterned activity in the circuit, and long depolarizations induced sustained patterned activity. The phase relationships, duration and frequency of simulated electrical activity in the network model were very similar to empirical observations and indicated that such a circuit could account for many features of patterned electrical activity in the isolated buccal ganglia. In addition, the possible involvement of catecholamines in regulating activity of this CPG was examined. Dopamine or its metabolic precursor L-3, 4-dihydroxyphenylalanine (DOPA) elicited sustained rhythmic neural activity in isolated buccal ganglia. A newly identified catecholaminergic interneuron, B65, was found to be rhythmically active in presence of DOPA, in response to radula nerve stimulation, as well as during its direct depolarization, which in turn elicited rhythmic activity in the CPG similar to that induced by DOPA. Finally, perfusion of semi-intact preparations with DOPA initiated rhythmic feeding movements indicative of ingestive behaviours.

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