Synaptic differentiation of single descending fibers studied by triple intracellular recording in the frog spinal cord.

Evoked excitatory postsynaptic potentials (EPSPs) were simultaneously intracellularly recorded in two lumbar motoneurons located in spinal segments 8-10 in response to intraaxonal stimulation of a descending fiber. Their mean amplitudes, paired-pulse facilitation, and short- and long-term posttetanic potentiation were compared to reveal possible functional differences among synapses formed by one axon on different postsynaptic targets. The mean amplitudes of EPSPs recorded in two motoneurons were significantly different in most experiments. This amplitude difference was related to the location of motoneurons in that it was twofold larger in motoneurons separated by >1 mm than in motoneurons located within 200 micron m of one another and also that the amplitude of EPSPs recorded in motoneurons located in the tenth segment was regularly smaller than the amplitude recorded in the ninth segment. The estimation of binomial model parameters suggests that the difference in mean EPSP amplitude was due mostly to differences in the maximal number of quanta prepared for release (binomial parameter N) and in mean release probability rather than to differences in quantal size. The ability of connections formed by a single axon on different motoneurons to undergo use-dependent synaptic modulations was different on scales of milliseconds, seconds, and tens of minutes as revealed by the measurements of effects of paired-pulse and tetanic stimulation. The difference in magnitude of short-term posttetanic potentiation in connections formed by a single descending axon was significantly correlated with the difference in mean probability of release in these connections. Thus our data revealed a functional nonuniformity of synapses formed by individual descending fibers on widely separated motoneurons, most likely innervating different muscles. This process can be one of the mechanisms by which a fine descending control of recruitment of motoneuronal populations is achieved.