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The Journal of Neuroscience, June 8, 2005, 25(23):5623-5637; doi:10.1523/JNEUROSCI.5305-04.2005

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Behavioral/Systems/Cognitive
Synaptic Facilitation and Behavioral Dishabituation in Aplysia: Dependence on Release of Ca²⁺ from Postsynaptic Intracellular Stores, Postsynaptic Exocytosis, and Modulation of Postsynaptic AMPA Receptor Efficacy

Quan Li,^1 * Adam C. Roberts,^2 * and David L. Glanzman^1,3

¹Department of Physiological Science and ²Interdepartmental PhD Program in Molecular, Cellular, and Integrative Physiology, University of California Los Angeles, Los Angeles, California 90095-1606, and ³Department of Neurobiology and Brain Research Institute, David Geffen School of Medicine at University of California Los Angeles, Los Angeles, California 90095-1761

Sensitization and dishabituation of the defensive withdrawal reflex in Aplysia have been ascribed to presynaptic mechanisms, particularly presynaptic facilitation of transmission at sensorimotor synapses in the CNS of Aplysia. Here, we show that facilitation of sensorimotor synapses in cell culture during and after serotonin (5-HT) exposure depends on a rise in postsynaptic intracellular Ca²⁺ and release of Ca²⁺ from postsynaptic stores. We also provide support for the idea that postsynaptic AMPA receptor insertion mediates a component of synaptic facilitation by showing that facilitation after 5-HT offset is blocked by injecting botulinum toxin, an exocytotic inhibitor, into motor neurons before application of 5-HT. Using a reduced preparation, we extend our results to synaptic facilitation in the abdominal ganglion. We show that tail nerve shock-induced facilitation of siphon sensorimotor synapses also depends on elevated postsynaptic Ca²⁺ and release of Ca²⁺ from postsynaptic stores and recruits a late phase of facilitation that involves selective enhancement of the AMPA receptor-mediated synaptic response. To examine the potential role of postsynaptic exocytosis of AMPA receptors in learning in Aplysia, we test the effect of injecting botulinum toxin into siphon motor neurons on dishabituation of the siphon-withdrawal reflex. We find that postsynaptic injections of the toxin block dishabituation resulting from tail shock. Our results indicate that postsynaptic mechanisms, particularly Ca²⁺-dependent modulation of AMPA receptor trafficking, play a critical role in synaptic facilitation as well as in dishabituation and sensitization in Aplysia.

Key words: Aplysia; sensitization; dishabituation; serotonin; intracellular calcium stores; AMPA receptor trafficking

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Received Aug 27, 2004; revised May 4, 2005; accepted May 5, 2005.

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