Electrotonic coupling in the inferior olivary (IO) nucleus is assumed to play a crucial role in generating the subthreshold membrane potential oscillations in olivary neurons and in synchronizing climbing fiber input into the cerebellar cortex. We studied the strength and spatial distribution of the coupling by simultaneous double patch recordings from olivary neurons in the brain slice preparation. Electrotonic coupling was observed in 50% of the cell pairs. The coupling coefficient (CC), defined as the ratio between voltage responses of the post- and the prejunctional cell, varied between 0.002 and 0.17; most of the pairs were weakly coupled. In more than 75% of the pairs, the CC was <0.05. The coupling resistance varied between 0.7 to 19.8 G(Omega), and 68% of the values fell between 0.7 to 8 G(Omega). The difference between the coupling coefficient measured on stimulation of cell 1 or cell 2 of a coupled pair was 27 +/- 16%. Direct calculation of the coupling resistance revealed an asymmetry of 24 +/- 12%, suggesting a directional preference of coupling. The coupling was voltage independent, although depolarization of either the pre- or the postjunctional neuron reduced the CC. The chance of a cell pair being coupled was 80% in immediate neighboring cells, but dropped to about 30% at a distance of 40 microm. No coupled pairs were observed at distances larger than 70 microm. In 52% of staining experiments neurobiotin injection into an olivary neuron produced indirect labeling of 1-11 nearby cells with an average of 3.8 +/- 2.9. All indirectly labeled cells were found in, or immediately adjacent, to the dendritic field of the directly stained neuron. Two distinct morphological types of olivary neurons, "curly" and "straight" cells, were found. In each case all neurons stained indirectly by dye passage through gap junctions belonged to the same type. Using the physiological data we estimated that each olivary neuron is directly coupled to about 50 neurons. Since somatic recordings may not reveal coupling through remote dendrites, we conclude that each neuron is directly connected to > or =50 neurons forming two distinct networks of curly and straight cells.