1. The synaptic activation by mossy fibers (MFs) of unipolar brush cells (UBCs) 
in the vestibular cerebellum (nodulus and uvula) was examined using patch-clamp 
recording methods in thin, rat cerebellar slices with Lucifer yellow-filled 
pipettes for subsequent fluorescence microscopic verification of the cell 
morphology. 2. UBCs were distinguished from adjacent granule cells in thin 
cerebellar slices in the uvula and nodulus regions by their larger soma 
diameters and short dendritic brush, greater whole-cell capacitance, and a 
prolonged, biphasic excitatory postsynaptic current (EPSC) to stimulation of 
MFs. 3. Thin-section transmission electron micrographs of the MF-UBC synapse 
displayed an unusually extensive area of synaptic apposition estimated to 
measure 12-40 microns2. The majority of UBCs was innervated by a single MF. At 
high magnification, individual clusters of presynaptic vesicles could be 
discerned, separated by regions of presynaptic membrane lacking vesicles, but 
apposed to continuous regions of postsynaptic density. Thus, after release, 
transmitter diffusion from the synaptic cleft must traverse considerable 
stretches of postsynaptic membrane before escape into extracellular space. In 
contrast, MF-granule cell synapses in these cerebellar regions resembled 
glutamate synapses in other brain regions in that the total synaptic area 
measured < or = 4 microns2. These synaptic junctions were flanked by short 
stretches of unspecialized plasma membrane, providing a short (0.5 micron) 
diffusional path from the site of neurotransmitter release to a branch point of 
the extracellular space. 4. The MF-evoked EPSC in UBCs was composed of a fast 
(10-90% rise time: 0.70 ms) and slow (10-90% rise time: 395 ms; 10-90% decay 
time: 3.1 s) component. The fast component was blocked by the 
alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate (AMPA/KA) 
antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (10 microM) and displayed linear 
current-voltage (I-V) relations in the presence or absence of external 
magnesium. 5. The slow EPSC was also mediated by glutamate receptors, but in 
most neurons both AMPA/KA and N-methyl-D-aspartate (NMDA) receptors contributed 
to the slow EPSC, with the contribution of NMDA receptors predominating in the 
majority of cells. Consequently, although all cells displayed linear I-V 
relations in Mg(2+)-free saline, cells in which the slow EPSC was predominently 
mediated by NMDA receptors exhibited voltage-dependent rectification in the 
presence of external Mg2+ (1 mM). 6. With increasing postnatal age (10-30 d), 
the contribution made to the slow EPSC by NMDA receptors declined, with a 
reciprocal increase in the contribution being made by AMPA/KA 
receptors.(ABSTRACT TRUNCATED AT 400 WORDS)