Neurotransmitter secretion along growing nerve processes: Comparison with synaptic vesicle exocytosis

In mature neurons, synaptic vesicles continuously recycle within the presyn aptic nerve terminal. In developing axons which are free of contact with a postsynaptic target, constitutive membrane recycling is not localized to th e nerve terminal; instead, plasma membrane components undergo cycles of exo endocytosis throughout the whole axonal surface (Matteoli et al., 1992; Kra szewski et al., 1995). Moreover, in growing Xenopus spinal cord neurons in culture, acetylcholine (ACh) is spontaneously secreted in the quantal fashi on along the axonal shaft (Evers et al., 1989; Antonov et al., 1998). Here we demonstrate that in Xenopus neurons ACh secretion is mediated by vesicle s which recycle locally within the axon. Similar to neurotransmitter releas e at the presynaptic nerve terminal, ACh secretion along the axon could be elicited by the action potential or by hypertonic solutions. We found that the parameters of neurotransmitter secretion at the nerve terminal and at t he middle axon were strikingly similar. These results lead us to conclude t hat, as in the case of the presynaptic nerve terminal, synaptic vesicles in volved in neurotransmitter release along the axon contain a complement of p roteins for vesicle docking and Ca2+-dependent fusion. Taken together, our results support the idea that, in developing axone, the rudimentary machine ry for quantal neurotransmitter secretion is distributed throughout the who le axonal surface. Maturation of this machinery in the process of synaptic development would improve the fidelity of synaptic transmission during high -frequency stimulation of the presynaptic cell.