There is increasing evidence that the various types of hippocampal nonpyramidal neurons control the principal cells in different ways. In the present study a type of spiny nonpyramidal cell in stratum lucidum of rat hippocampal region CA3 was studied by Golgi impregnation. Three Golgi-impregnated and gold-toned neurons of this type were further analyzed by electron microscopy and postembedding immunocytochemistry. The dendrites of these bipolar neurons seemed to be restricted to stratum lucidum and ran parallel with the mossy fibers that terminate in this layer. A characteristic feature of this neuron is the presence of long, thin spines on both cell body and dendrites. Although these dendrites were exposed to a large number of mossy fibers, no thorny excrescences were formed which are characteristic postsynaptic elements of CA3 pyramidal neurons for synaptic contact with the mossy fibers. Semithin sections of Golgi-impregnated and gold-toned stratum lucidum cells displayed immunoreactivity of the cell body region for glutamate but not for GABA. A fine-structural analysis of gold-toned sections revealed a large cell body with numerous cytoplasmic organelles and an indented nucleus. Numerous asymmetric synapses were found on dendritic shafts as well as on the long, thin somatic and dendritic spines. Usually, several presynaptic boutons contacted a single spine. The majority of these asymmetric spine synapses were probably of mossy fiber origin, although no giant mossy fiber synapses were formed. The long spines were contacted by much smaller en passant synapses of preterminal axons. In contrast, giant mossy fiber boutons were found presynaptic to dendritic shafts and cell bodies of these cells. Our morphological analysis of a glutamate-immunoreactive, GABA-negative type of nonpyramidal neuron that receives convergent mossy fiber input suggests that the impulse flow within the "trisynaptic pathway" is more complex than previously assumed.