Maintenance of long-term adaptation of synaptic transmission requires axonal transport following induction in an identified crayfish motoneuron

Abstract

Motoneurons can adapt to altered levels of electrical activity by effecting semi-permanent changes in their neuromuscular synaptic physiology. In the present study, we tested the hypothesis that maintenance of activity-dependent long-term adaptation of synaptic transmission in a crayfish abdominal extensor motoneuron (phasic axon 3) required axonal transport following induction. Intact crayfish were chronically wired for periodic in vivo stimulation of axon 3. Periodic unilateral stimulation for 3–5 consecutive days (2 h/day) induced long-term adaptation (LTA) of neuromuscular synaptic transmission in axon 3. Initial EPSP amplitudes (measured at 0.1 Hz) were significantly reduced to approximately 40% of contralateral control amplitudes over a 7-day poststimulation period. Additionally, synaptic depression during 5 Hz test stimulation of axon 3 was significantly less in chronically stimulated neurons: excitatory postsynaptic potential (EPSP) amplitudes measured after 20 min of 5 Hz test stimulation (final EPSPs) were significantly larger in conditioned neurons than in unstimulated controls. The depression of initial EPSP amplitudes persisted for 7 days postinduction, while the increased synaptic stamina persisted for 4 days but was absent at 7 days postinduction. Axotomy of axon 3 following induction of LTA had no effect on long-term maintenance of the activity-induced reduction in initial EPSP amplitudes. Initial EPSP amplitudes in conditioned, axotomized neurons were still reduced to 42% of control amplitudes over the 7-day postinduction period. In contrast, postinduction axotomy of axon 3 elicited an accelerated decay of the enhanced synaptic stamina. Following axotomy, final EPSP amplitudes were significantly larger in conditioned neurons for only 1 day poststimulation. At all other times tested (2, 4, and 7 days postinduction), final EPSP amplitudes measured from conditioned, axotomized neurons were not significantly different from those measured from contralateral, unstimulated, intact neurons. Unilateral axotomy of axon 3 per se, without any conditioning stimulation, produced no marked changes in initial and final EPSP amplitudes over the time course of these experiments (8 days). These experiments establish that full maintenance of long-term adaptation of synaptic transmission in axon 3 required an intact axonal connection between the soma and neuromuscular synapses of axon 3. Furthermore, the results indicate that axonal transport of macromolecules derived from the cell body of axon 3 is not required for persistence of the long-term depression of initial EPSP amplitudes, while maintenance of the synaptic stamina required such transport.