Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia

Abstract

We have identified the processes of mechanoreceptor sensory neurons by intracellular injection of horseradish peroxidase in order to study the structure of synapses which exhibit profound, behaviourally-relevant plasticity. These synapses are located at small, varicose expansions along or at the end of the fine, microtubule-containing neurites, and they are crowded with vesicles some of which are associated with the varicosity membrane at regions of membrane specialization morphologically equivalent to active zones described in other species. These active zones occur between pre- and postsynaptic processes at two varieties of apposition: a conventional flat one, and a more elaborate indented one. At indented appositions, the presynaptic varicosity is invaginated by a thin (less than 0.25 micrometer diameter) spine of variable length. The active zones of indented synapses have approximately twice the vesicle frequency of flat synapses, suggesting that indented synapses are more effective. Sensory neuron terminals are relatively uniform in their structure, having similar concentrations of vesicles and numbers of active zones, and the majority of the processes postsynaptic to them are less than 0.5 micrometer in diameter. These regularities, and the presence of two strikingly-different types of synaptic apposition, flat and indented, should facilitate structural comparisons of neurons from naive and behaviourally-modified animals. The possible dynamic interconversion of indented and flat appositions at the synaptic terminals of sensory neurons and its behavioural relevance are discussed.