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The Journal of Neuroscience, August 23, 2006, 26(34):8662-8671; doi:10.1523/JNEUROSCI.2307-06.2006

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Cellular/Molecular
The Circadian Clock Modulates Core Steps in Long-Term Memory Formation in Aplysia

Lisa C. Lyons, Maria Sol Collado, Omar Khabour, Charity L. Green, and Arnold Eskin

Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204-5001

Correspondence should be addressed to Dr. Arnold Eskin, Department of Biology and Biochemistry, University of Houston, 369 Science and Research II, Houston, TX 77204-5001. Email: eskin{at}uh.edu

The circadian clock modulates the induction of long-term sensitization (LTS) in Aplysia such that long-term memory formation is significantly suppressed when animals are trained at night. We investigated whether the circadian clock modulated core molecular processes necessary for memory formation in vivo by analyzing circadian regulation of basal and LTS-induced levels of phosphorylated mitogen-activated protein kinase (P-MAPK) and Aplysia CCAAT/enhancer binding protein (ApC/EBP). No basal circadian regulation occurred for P-MAPK or total MAPK in pleural ganglia. In contrast, the circadian clock regulated basal levels of ApC/EBP protein with peak levels at night, antiphase to the rhythm in LTS. Importantly, LTS training during the (subjective) day produced greater increases in P-MAPK and ApC/EBP than training at night. Thus, circadian modulation of LTS occurs, at least in part, by suppressing changes in key proteins at night. Rescue of long-term memory formation at night required both facilitation of MAPK and transcription in conjunction with LTS training, confirming that the circadian clock at night actively suppresses MAPK activation and transcription involved in memory formation.

The circadian clock appears to modulate LTS at multiple levels. 5-HT levels are increased more when animals receive LTS training during the (subjective) day compared with the night, suggesting circadian modulation of 5-HT release. Circadian modulation also occurred downstream of 5-HT release because animals treated with 5-HT to induce LTS exhibited significantly greater LTS when treated during the (subjective) day compared with the night. Together, our studies suggest that the circadian clock modulates LTS at multiple steps and locations during the formation of long-term memory.

Key words: Aplysia; C/EBP; circadian rhythm; MAP kinase; learning and memory; serotonin

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Received Jan. 3, 2006; revised July 14, 2006; accepted July 15, 2006.

Correspondence should be addressed to Dr. Arnold Eskin, Department of Biology and Biochemistry, University of Houston, 369 Science and Research II, Houston, TX 77204-5001. Email: eskin{at}uh.edu

This article has been cited by other articles:

				J. R. Gerstner, L. C. Lyons, K. P. Wright Jr, D. H. Loh, O. Rawashdeh, K. L. Eckel-Mahan, and G. W. Roman Cycling Behavior and Memory Formation J. Neurosci., October 14, 2009; 29(41): 12824 - 12830. [Abstract] [Full Text] [PDF]

				A. I. Hernandez, J. Wolk, J.-Y. Hu, J. Liu, T. Kurosu, J. H. Schwartz, and S. Schacher Poly-(ADP-Ribose) Polymerase-1 Is Necessary for Long-Term Facilitation in Aplysia J. Neurosci., July 29, 2009; 29(30): 9553 - 9562. [Abstract] [Full Text] [PDF]

				L. C. Lyons and G. Roman Circadian modulation of short-term memory in Drosophila Learn. Mem., December 30, 2008; 16(1): 19 - 27. [Abstract] [Full Text] [PDF]

				L. C. Lyons, C. L. Green, and A. Eskin Intermediate-Term Memory is Modulated by the Circadian Clock J Biol Rhythms, December 1, 2008; 23(6): 538 - 542. [Abstract] [PDF]

				D. Levitan, L. C. Lyons, A. Perelman, C. L. Green, B. Motro, A. Eskin, and A. J. Susswein Training with inedible food in Aplysia causes expression of C/EBP in the buccal but not cerebral ganglion Learn. Mem., May 28, 2008; 15(6): 412 - 416. [Abstract] [Full Text] [PDF]

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