The architecture of neurosecretory cells (NSCs) from each of two bilaterally symmetrical clusters of somata in the brain of the moth, Manduca sexta, was determined by intracellular injection of Lucifer Yellow and horseradish peroxidase. Furthermore, the ionic basis of the action potential in these cells was examined. NSC somata were visualized in the desheathed pupal protocerebrum by their reflective opalescence under direct fiberoptic illumination. Intracellular staining revealed at least six morphological classes of monopolar neurons distinguishable by the size and position of their somata as well as the patterns of their dendritic fields, axonal pathways, and terminal projections. The number of morphological classes of NSCs is in accord with the estimated number of brain neurohormones--a finding that suggests a different neuroendocrine function for each class. The observed overlap of dendritic fields is consistent with synaptic interaction among NSCs or the sharing of common inputs. Finally, the demonstration of terminal ramifications and varicosities in the corpora cardiaca and corpora allata confirms that these are the neurohemal organs for cerebral NSCs. Intracellular recordings revealed that the NSC somata had resting membrane potentials of 35 to 45 mV and were electrically excitable; they showed broad (10 to 20 msec) overshooting action potentials, long hyperpolarizing afterpotentials, and postsynaptic potentials. Impulse amplitude was maintained in the absence of external sodium or in the presence of 10(-5)M tetrodotoxin, but impulses were completely and reversibly blocked by 10 mM cobalt. Postsynaptic potentials were blocked by all three conditions. These results indicate that impulses in the somata are generated primarily by calcium inward currents. Cations, tetrodotoxin, and horseradish peroxidase in the bathing medium did not readily exchange with the extracellular space of the desheathed brain. However, light protease treatment of the brain facilitated ion exchange. These findings provide evidence for the persistence of a blood-brain barrier even in desheathed ganglia.