Modulation of monosynaptic excitation in the neonatal rat spinal cord

1. The effects of high-frequency (5-50 Hz) stimulation of dorsal root afferents on monosynaptic excitation of α motoneurons was studied in the in vitro spinal cord preparation of the neonatal rat, using sharp-electrode intracellular recordings. 2. Double pulse stimulation of dorsal root afferents induced severe depression of testing excitatory postsynaptic potentials (EPSPs) at each of the tested interstimulus intervals (15 ms-5 s). After perfusion of the preparation with low-calcium, high-magnesium Krebs saline, the amplitude of the conditioning EPSPs was markedly decreased and the testing EPSPs exhibited substantial facilitation that was maximal at the 20-ms interval and that was accompanied by depression at intervals ≥60- 100ms. 3. Short-duration stimulus trains applied to dorsal root afferents normally induced tetanic depression of the intracellularly recorded monosynaptic EPSPs. Switching the bathing solution to low-calcium, high- magnesium saline decreased the control EPSP and induced facilitation and then tetanic potentiation (TP) of the EPSPs within the applied train. The magnitude of potentiation (% potentiation) of these EPSPs depended on the interpulse interval of the short stimulus train and on the degree of attenuation of the unpotentiated control EPSP after the solution was changed from normal- to low-calcium Krebs solution. 4. Long-duration stimulus trains applied to dorsal root afferents at 5-10 Hz induced marked depression of monosynaptic EPSPs during the train. The depression was alleviated after cessation of the tetanic stimulation and was followed in some cases by slight posttetanic potentiation. Perfusion of the preparation with low-calcium, high-magnesium solution reduced the amplitude of the pretetanic EPSPs and induced moderate potentiation or slight depression during the tetanic train. After the tetanic train, EPSPs exhibited posttetanic potentiation (PTP) that lasted ≤10 min. 5. On the basis of these results, it is suggested that monosynaptic EPSPs produced by dorsal root afferents in the neonatal rat spinal cord are modulated simultaneously (as in the adult spinal cord) by processes acting to increase the EPSP amplitude (facilitation, TP, and PTP) and to decrease it (depression). Unlike the adult spinal cord, the immature transmitter release machinery of the developing spinal cord imposes, under normal conditions, a prolonged synaptic depression that masks facilitation and TP but allows occasionally the expression of moderate PTP. Substantial expression of facilitation TP and PTP is revealed only by conditions that decrease calcium influx to presynaptic terminals, and, concomitantly, transmitter release. The long duration of PTP in low-calcium solution in the neonatal rat may be attributed to slower kinetics of processes involved in extrusion and intraterminal buffering of calcium in the developing mammalian spinal cord.