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The Journal of Neuroscience, June 11, 2008, 28(24):6220-6230; doi:10.1523/JNEUROSCI.2935-07.2008

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Behavioral/Systems/Cognitive
A Novel Conditional Genetic System Reveals That Increasing Neuronal cAMP Enhances Memory and Retrieval

Carolina Isiegas,¹ Conor McDonough,¹ Ted Huang,¹ Robbert Havekes,¹ Sara Fabian,¹ Long-Jun Wu,² Hui Xu,² Ming-Gao Zhao,² Jae-Ick Kim,³ Yong-Seok Lee,³ Hye-Ryeon Lee,³ Hyoung-Gon Ko,³ Nuribalhae Lee,³ Sun-Lim Choi,³ Jeong-Sik Lee,^4,5 Hyeon Son,^4,5 Min Zhuo,² Bong-Kiun Kaang,³ and Ted Abel¹

¹Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, ²Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada M5S 1A8, ³National Creative Research Initiative Center for Memory, Department of Biological Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, South Korea and Departments of ⁴Biochemistry and ⁵Molecular Biology, Hanyang University College of Medicine, Seoul 133-791, South Korea

Correspondence should be addressed to Carolina Isiegas, Bong-Kiun Kaang, or Ted Abel at the above addresses. Email: cisiegas{at}sas.upenn.edu, Email: kaang{at}snu.ac.kr, or Email: abele{at}sas.upenn.edu

Consistent evidence from pharmacological and genetic studies shows that cAMP is a critical modulator of synaptic plasticity and memory formation. However, the potential of the cAMP signaling pathway as a target for memory enhancement remains unclear because of contradictory findings from pharmacological and genetic approaches. To address these issues, we have developed a novel conditional genetic system in mice based on the heterologous expression of an Aplysia octopamine receptor, a G-protein-coupled receptor whose activation by its natural ligand octopamine leads to rapid and transient increases in cAMP. We find that activation of this receptor transgenically expressed in mouse forebrain neurons induces a rapid elevation of hippocampal cAMP levels, facilitates hippocampus synaptic plasticity, and enhances the consolidation and retrieval of fear memory. Our findings clearly demonstrate that acute increases in cAMP levels selectively in neurons facilitate synaptic plasticity and memory, and illustrate the potential of this heterologous system to study cAMP-mediated processes in mammalian systems.

Key words: cAMP; conditional genetic system; octopamine; synaptic plasticity; memory; retrieval

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Received June 28, 2007; revised April 9, 2008; accepted April 29, 2008.

Correspondence should be addressed to Carolina Isiegas, Bong-Kiun Kaang, or Ted Abel at the above addresses. Email: cisiegas{at}sas.upenn.edu, Email: kaang{at}snu.ac.kr, or Email: abele{at}sas.upenn.edu

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