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The Journal of Neuroscience, March 23, 2005, 25(12):3168-3180; doi:10.1523/JNEUROSCI.4908-04.2005

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Cellular/Molecular
Phosphorylation-Dependent Low-Frequency Depression at Phasic Synapses of a Crayfish Motoneuron

Lorelei B. Silverman-Gavrila, Peter M. R. Orth, and Milton P. Charlton

Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5S 1A8

Extremes in presynaptic differentiation can be studied at the crayfish leg extensor muscle where, on the same muscle fiber, one motoneuron makes "phasic" depressing synapses that have a high probability of neurotransmitter release and another motoneuron makes "tonic," low-probability, facilitating synapses. The large motor axons permit intracellular access to presynaptic sites. We examined the role of phosphorylation during low-frequency depression (LFD) in the relatively little studied phasic synapses.

LFD occurs with stimulation at 0.2 Hz and develops with time constants of 4 and 105 min to reach >50% depression of transmitter release in 60 min similar to long-term depression in mammals. LFD is not associated with changes in postsynaptic sensitivity to transmitter and thus is a presynaptic event, although it is not accompanied by changes in the presynaptic action potential. Blockade of protein kinases accelerated the slow phase of LFD, but stimulation of kinases reduced depression. Blockade of protein phosphatases 1A/2A reversed the slow phase. When calcineurin was inhibited, both phases of LFD were abolished, and facilitation occurred instead. Immunostaining showed calcineurin-like immunoreactivity in synaptic terminals. Recovery from LFD occurred in 1 h if stimulation frequency was reduced to 0.0016 Hz. Recovery was blocked by kinase inhibition.

This study shows that phosphorylation-dependent mechanisms are involved in LFD and suggests that exocytosis is controlled by conditions that shift the balance between phosphorylated and unphosphorylated substrates. The shift can occur by alteration in the relative activities of protein kinases and phosphatases.

Key words: synaptic plasticity; low-frequency depression; protein kinase A; protein kinase C; calcineurin; presynaptic differentiation

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Received June 30, 2004; revised February 11, 2005; accepted February 15, 2005.

This article has been cited by other articles:

				G. Srinivasan, J. H. Kim, and H. von Gersdorff The Pool of Fast Releasing Vesicles Is Augmented by Myosin Light Chain Kinase Inhibition at the Calyx of Held Synapse J Neurophysiol, April 1, 2008; 99(4): 1810 - 1824. [Abstract] [Full Text] [PDF]

				J. E. R. Wilkerson, I. Satriotomo, T. L. Baker-Herman, J. J. Watters, and G. S. Mitchell Okadaic Acid-Sensitive Protein Phosphatases Constrain Phrenic Long-Term Facilitation after Sustained Hypoxia J. Neurosci., March 12, 2008; 28(11): 2949 - 2958. [Abstract] [Full Text] [PDF]

				L. Silverman-Gavrila and R. Silverman-Gavrila Depression in the Fly J. Neurosci., August 2, 2006; 26(31): 8021 - 8022. [Full Text] [PDF]

				O. Zamir and M. P. Charlton Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions J. Physiol., February 15, 2006; 571(1): 83 - 99. [Abstract] [Full Text] [PDF]

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