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The Journal of Neuroscience, October 22, 2003, 23(29):9585-9594

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Behavioral/Systems/Cognitive
Prolonged Habituation of the Gill-Withdrawal Reflex in Aplysia Depends on Protein Synthesis, Protein Phosphatase Activity, and Postsynaptic Glutamate Receptors

Youssef Ezzeddine¹ and David L. Glanzman^1,2

¹Department of Physiological Science and ²Department of Neurobiology and the Brain Research Institute, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095

Despite representing perhaps the simplest form of memory, habituation is not yet well understood mechanistically. We used a reduced preparation to analyze the neurobiological mechanisms of persistent habituation of a simple behavior, the defensive withdrawal reflex of the marine snail Aplysia californica. This preparation permits direct infusion of drugs into the abdominal ganglion during training via a cannula in the abdominal artery. Using siphon-elicited gill withdrawal, we demonstrate habituation of withdrawal that persists for 1-6 hr after repeated, spaced blocks of habituating stimulation. This form of habituation exhibits site specificity and requires protein synthesis because it is blocked by the presence of anisomycin, a protein synthesis inhibitor. We also find that habituation of gill withdrawal requires protein phosphatase activity, because it is blocked by okadaic acid, an inhibitor of protein phosphatase. Finally, habituation of gill withdrawal requires activation of NMDA-type and AMPA-type postsynaptic receptors within the abdominal ganglion, because it is blocked by infusion of DL-2-amino-5-phosphonovaleric acid or 6,7-dinitroquinoxaline-2,3-dione. The requirement for activation of postsynaptic glutamatergic receptors indicates that homosynaptic depression, an exclusively presynaptic mechanism that has been implicated previously in habituation in Aplysia, does not play a significant role in persistent habituation of the withdrawal reflex. Our results indicate that postsynaptic mechanisms, possibly including modulation of glutamate receptor function, play a major, heretofore unsuspected, role in habituation in Aplysia.

Key words: Aplysia; habituation; long-term memory; protein synthesis; protein phosphatase; okadaic acid; APV; NMDA; AMPA; DNQX; glutamate receptors; postsynaptic processes; LTD

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Received May 12, 2003; revised August 15, 2003; accepted August 28, 2003.

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