With the use of an isolated, perfused ganglion preparation from the tobacco hornworm, Manduca sexta, we have examined the responses of an identified proleg retractor motoneuron (designated PPR) to trains of stimuli delivered to sensory branches of the ventral nerve (VN). 2. Trains of stimuli (50 Hz, 100 ms to 5 s) delivered to the proleg sensory nerve, VNA, caused PPR to depolarize and initiate a bout of spiking activity that outlasted the stimulus. A fast component of this response was due to monosynaptic input from planta hair sensory neurons, acting on nicotinic acetylcholine receptors (nAChRs). The fast response to VNA stimulation was abolished when the ganglion was treated with the nicotinic antagonist, mecamylamine, leaving a slow, long-lasting depolarization of PPR, which we have called the slow excitatory postsynaptic potential (sEPSP). 3. A sEPSP could be evoked by stimulation of all the major subbranches of VNA ipsilateral to PPR's cell body. Small sEPSPs were also evoked by stimulation of all but one of the major contralateral subbranches of VNA. 4. During a sEPSP the spike threshold of PPR became more negative. This increase in excitability was not correlated with changes in membrane potential measured at the cell body, and there was no detectable change in input resistance. We conclude that the spike-threshold change reflects either a depolarization electrically remote from the cell body, or a change in PPR's spike initiation properties that are not reflected in the membrane potential. 5. Both the sEPSP and the associated change in PPR's spike threshold were blocked by several muscarinic antagonists. Scopolamine was effective at concentrations > 2 x 10(-7) M, atropine at concentrations > 1 x 10(-6) M, and pirenzepine at 5 x 10(-5) M. 4-Diphenylacetoxy-N-methylpiperidine (4-DAMP), methoctramine, hexahydrosiladifenidol, and AF-DX 116 were all poor antagonists. 6. Bath application of the muscarinic agonist oxotremorine-M (oxo-M) at concentrations > 3 x 10(-7) M increased the spontaneous spiking activity of PPR and other proleg motoneurons. In PPR, this increased activity was accompanied by a small depolarization and a more negative spike threshold, both of which were inhibited by 1 x 10(-7) M scopolamine. 7. At concentrations > 6 x 10(-8) M, bath-applied oxo-M depolarized PPR even when spike activity in the ganglion was blocked with tetrodotoxin. During such spike blockage, pressure ejection of brief puffs of oxo-M into the neuropil evoked a long-lasting depolarization of PPR that resembled the sEPSP.(ABSTRACT TRUNCATED AT 400 WORDS)
