Structural plasticity at identified synapses during long‐term memory in Aplysia

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Abstract
We have used the gill‐ and siphon‐withdrawal reflex of Aplysia californica to determine the morphological basis of the prolonged changes in synaptic effectiveness that underlie long‐term habituation and sensitization. We have found that clear structural changes accompany behavioral modification and have demonstrated that these can be detected at the level of identified sensory neuron synapses, a critical site of plasticity for the short‐term forms of both types of learning. These alterations occur at two different levels of synaptic organization and include (1) changes in focal regions of synaptic membrane specialization—the number, size and vesicle complement of sensory neuron active zones are larger in sensitized animals and smaller in habituated animals compared with controls—and (2) a parallel but more dramatic and global trend involving modulation of the total number of presynaptic varicosities per sensory neuron. Quantitative analysis of the time course over which these structural alterations occur during sensitization has further demonstrated that changes in the number of varicosities and active zones persist in parallel with the behavioral retention of the memory. This increase in the number of sensory neuron synapses during long‐term sensitization in Aplysia is similar to changes in the number of synapses in the mammalian brain following various forms of environmental manipulations and learning (Greenough, 1984). Therefore learning may involve a form of neuronal growth across a braod segment of the animal kingdom, thereby suggesting a role for structural synaptic plasticity during long‐term behavioral modifications.