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Journal of Neuroscience, Vol 16, 425-435, Copyright © 1996 by Society for Neuroscience

ARTICLE

Presynaptic facilitation revisited: state and time dependence

JH Byrne and ER Kandel
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77030, USA.

The mechanisms underlying short-term presynaptic facilitation, the enhancement of transmitter release from sensory neurons in Aplysia, induced by serotonin (5-HT), can be divided into two categories: (1) changes in ionic conductances leading to spike broadening and enhancement of Ca2+ influx; and (2) actions on the machinery for transmitter release that are independent of spike broadening and the resulting increases in Ca2+ influx. Spike broadening and the associated enhancement of excitability are induced by the modulation of K+ conductances in the sensory neuron. The cellular mechanisms that contribute to the enhancement of release that is independent of spike broadening are not known and may involve vesicle mobilization or other steps in exocytotic release. These two facilitatory actions of 5-HT are mediated by at least two second-messenger-activated protein kinase systems, protein kinase A (PKA) and protein kinase C (PKC). These two second-messenger cascades overlap in their contributions to synaptic facilitation. However, their relative contributions to enhancement of transmitter release are not simply synergistic but are state- and time- dependent. The state dependence is a reflection of the synapse's previous history of activity. When the synapse is rested (and not depressed), a brief pulse of 5-HT (lasting from 10 sec to 5 min) produces its actions primarily through PKA via both spike broadening- dependent and -independent mechanisms. The broadening primarily involves the modulation of a voltage-dependent K+ current, IKV, with a small contribution by a voltage-independent K+ current, IKS. By contrast, the enhancement of excitability is mediated primarily by the modulation of IKS. As the synapse becomes depressed with repeated activity, the contribution of PKC becomes progressively more important. As is the case with PKA, PKC produces its action both by broadening the spike via modulation of IKV and by a spike broadening-independent mechanism. In addition to being state-dependent, the mechanisms of facilitation are time-dependent. There are differences in the response to 5-HT when it is given briefly to produce short-term facilitation or when the exposure is prolonged. When exposure is brief (< or = 5 min), PKA dominates. When exposure is prolonged (10-20 min), PKC becomes dominant as it is with depressed synapses. Thus, synaptic plasticity appears to be expressed in several overlapping time domains, and the transition between very short-term facilitation and various intermediate duration phases seems to involve interactive processes between the kinases.

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