Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: Synaptic connections, effects on ongoing motor rhythms, and peptide modulation

M. R. Plummer, M. D. Kirk

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Abstract

1. Two buccal ganglia interneurons, labeled here as B51 and B52, have been identified on the basis of morphological and physiological criteria. 2. These neurons have multipolar cell bodies. B51 extends a major neurite, which arborizes in the neuropil ipsilateral to the soma; extends into the buccal commissure, where it branches profusely; and projects an axon out the radular nerve (n1); other processes emanating from the soma arborize in the adjacent cell body layer. B52 arborizes ipsilateral to its cell body and sends a major process out of the ipsilateral hemiganglion into the sheath that attaches the buccal ganglia to the buccal mass proper. Here the B52 axon projects through a previously undescribed structure, which forms an arch over the buccal commissure that we designate the commissural arch. The extraganglionic B52 axon sends several branches into the connective tissue and then returns to the contralateral hemiganglion, where it again branches. 3. Each neuron exhibits a unique set of physiological properties. B51 frequently produces plateau potentials, which persist and are even enhanced in solutions where Ca2+ is replaced with Co2+. On the other hand, B52 shows a powerful posthyperpolarization rebound that contributes to its burst formation during spontaneous and nerve-elicited cyclic motor output. 4. B51 and B52 display distinctive rhythmic bursting on stimulation of the radular nerve or esophageal nerve. Their burst-firing tended to occur at certain phase relationships with respect to firing in other buccal premotor and motor neurons. 5. When firing frequency is measured as a function of intracellularly injected current, B51 shows a steplike increase in firing with increasing current, whereas B52 firing frequency is continuously graded. 6. B51 and B52 were found to make extensive synaptic connections within the buccal ganglia. B51 exhibited primarily excitatory electrical connections with known premotor and motor neurons, including an electrotonic synapse with its contralateral homologue. 7. In contrast, B52 made bilateral inhibitory synapses with nearly all of the premotor and motor neurons of the ventral motor cluster. Most of these connections appeared to be monosynaptic, producing synaptic potentials with short and fixed latencies that persisted when the ganglia were bathed in solutions containing elevated concentrations of Ca2+ and Mg2+. 8. Other synaptic potentials produced by B52 were more variable in size and latency; these included slow inhibition of the B4 and B5 neurons and excitation of an identifiable neuron that projected out the radular nerve. The latter connection and a connection with its contralateral homologue were the only instances of excitation produced by B52. 9. B51 and B52 reciprocally inhibited each other. B52 produced large monosynaptic inhibitory postsynaptic potentials (IPSPs) in B51, whereas B51 caused an IPSP in B52 only after firing multiple spikes at high frequency, suggesting an indirect mechanism. 10. Activity in B51 and B52 was coordinated bilaterally because of common synaptic input and by direct and indirect electrical coupling across the midline. 11. Direct depolarization of B51 could elicit patterned buccal motor output and was capable of entraining ongoing patterned activity, suggesting that it interacted with a feeding central pattern generator (CPG). Directly firing B52 did not elicit any patterned motor output. 12. Motor output elicited by B51 was dramatically altered by bath application of the neuropeptide Small Cardioactive Peptide B (SCP(b)), with regular high-frequency bursts being recruited in the presence of the peptide. 13. B52 appeared to be directly depolarized by SCP(b) and exhibited a prolonged excitation that persisted in solutions containing high concentrations of divalent cations, which reduced polysynaptic input. 14. A combination of unique intrinsic properties and patterns of synaptic connections endow B51 and B52 with special roles in the control of cyclic bursting activity in the buccal ganglia. Although SCP(b) may act directly on B52, its ability to elicit patterened motor output appears to be due to actions on yet-unidentified members of buccal circuits underlying feeding motor programs.

Original languageEnglish (US)
Pages (from-to)539-558
Number of pages20
JournalJournal of neurophysiology
Volume63
Issue number3
DOIs
StatePublished - 1990
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

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