Maturation in properties of motoneurons and their segmental input in the neonatal rat

Abstract

1. The isolated neonatal rat spinal chord preparation was used to investigate the development of segmental afferent input to lumbar motoneourons during the first nine postnatal days. Motoneurons, identified with the use of antidromic stimulation of the ventral roots, were characterized electrophysiologically, and their synaptic input in response to stimulation of the homologous dorsal root was studied. 2. Motoneurons in postnatal day (P) 1–3 preparations exhibited lower rheobase and lower input conductance than those impaled in spinal cords taken from animals at P7-9. This finding is consistent with the increase in motoneuron size known to occur during this time. 3. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked at low-frequency (0.1-Hz) stimulation in high-Ca2+ saline exhibited no change in mean amplitude between P1-3 and P7-9 despite an increase in input conductance of the motoneurons, suggesting that some aspect of these synapses underwent a compensatory change. Polysynaptic EPSPs were smaller in the older animals. 4. When bursts of stimuli were delivered at higher frequencies ranging from 10 to 167 Hz, the EPSPs exhibited substantial depression. The depression of monosynaptic EPSPs was significantly less at P7-9 than at P1-3. Changing the bathing solution from a high-Ca2+ saline to a low-Ca2+/high-Mg2+ saline reduced the amplitude of the monosynaptic EPSP and made it less susceptible to depression during high-frequency stimulation. Facilitation of the evoked response, which has been observed in the adult rat, was never seen under any of these conditions. 5. Although synapses on high-rheobase motoneurons exhibited less depression than those on low-rheobase motoneurons, as anticipated from previous results in adults, the EPSPs at synapses on high-rheobase motoneurons tended to be larger in amplitude, not smaller as expected. This suggests that the specialization among synapses on motoneurons that exists in adults has not yet developed by P7-9. Instead, EPSP amplitude may be greater in motoneurons that have been growing rapidly, such as the high-rheobase motoneurons found during these stages of development. 6. Evidence is presented that the growing diversity shown in modulation behavior at the Ia afferent motoneuron synapse during the first postnatal week is determined primarily by motoneuron characteristics. It is speculated that as motoneurons grow during the immediate postnatal period, the presynaptic terminal regions of axons terminating on them become specialized to render the synapse less susceptible to depression. This specialization may be myelination of the afferent terminals or may perhaps be related to the transmitter release process itself. The adult distribution of depression develops later, presumably as the components of the monosynaptic reflex mature.