We have examined the various classes of cells that can be innervated by the giant cerebral neuron (GCN), an identified serotonergic cell that functions in arousal and maintenance of feeding behavior. We have found that this single neuron innervates a remarkable variety of postsynaptic targets by means of varicosities bearing active zones. The neuron's presynaptic terminals were identified by electron microscopic radioautography after intrasomatic injection of a tritiated amino sugar precursor of membrane glycoproteins; these are moved to nerve endings by fast axonal transport. In addition to endings on buccal muscle, we have found that GCN forms appositions with the morphological characteristics of synapses on axonal processes and cell bodies of neurons in the buccal ganglion and, unexpectedly, it forms appositions most often with glial cells which form the lining of intraganglionic hemal sinuses. Thus, GCN, through contacts on a variety of postsynaptic targets, has the potential of mediating several different functions, each of which is usually associated with a specific specialized type of neuron. In random electron micrographs, approximately 14% of GCN's varicosities had membrane specializations presumed to be the sites where transmitter is released. In these sections, GCN's active zones were quite small, 0.25 micrometer or approximately five vesicle diameters long. One of GCN's terminals was reconstructed completely from a series of thin sections. It had a single, flat ovoid active zone with an area of 17 micrometers2. We suggest that active zones often are overlooked in random sections of monoaminergic terminals because they are small.