The Journal of Neuroscience, January 28, 2009, 29(4):898-906; doi:10.1523/JNEUROSCI.4588-08.2009
Previous Article | Next Article 
Behavioral/Systems/Cognitive
Rapid Activation of Plasticity-Associated Gene Transcription in Hippocampal Neurons Provides a Mechanism for Encoding of One-Trial Experience
Teiko Miyashita,1
Stepan Kubik,1,3
Nahideh Haghighi,1
Oswald Steward,1,2 and
John F. Guzowski1
1Department of Neurobiology and Behavior, Center for the Neurobiology of Learning and Memory and 2Reeve-Irvine Research Center, Departments of Anatomy and Neurobiology, and Neurosurgery, University of California, Irvine, Irvine, California 92697, and 3Department of Neurophysiology of Memory, Institute of Physiology, Academy of Sciences of the Czech Republic, 14220 Prague, Czech Republic
Correspondence should be addressed to John F. Guzowski, 108 Bonney Research Labs, Irvine, CA 92697-3800. Email: john.g{at}uci.edu
The hippocampus is hypothesized to support rapid encoding of ongoing experience. A critical prerequisite for such function is the ability to readily recruit enduring synaptic plasticity in hippocampal neurons. Hippocampal long-term potentiation (LTP) and memory consolidation require expression of the immediate-early gene (IEG) Arc. To determine whether Arc transcription could be driven by limited and controlled behavioral experience, we used a rectangular track paradigm. In past electrophysiological studies, pyramidal neurons recorded from rats running in one direction on similar tracks typically exhibited a single firing field. Using fluorescence in situ hybridization, we show that the behavioral activity associated with a single lap around the track was sufficient to trigger Arc transcription in complete CA3 neuronal ensembles, as predicted given the role of CA3 in one-trial learning. In contrast, Arc transcription in CA1 ensembles was recruited incrementally, with maximal activation achieved after four laps a day for 4 consecutive days. To test whether Arc transcription is linked to learning and plasticity, or merely elicited by location-specific firing, we inactivated the medial septum, a treatment that compromises hippocampus-dependent learning and LTP but spares location-specific firing in CA1 neurons. Septal inactivation abolished track training-induced Arc transcription in CA1 and CA3 neurons, showing that Arc transcription requires plasticity-inducing stimuli. Accordingly, LTP induction activated Arc transcription in CA1 neurons in vivo. These findings demonstrate for the first time that a single brief experience, equivalent to a single crossing of a firing field, can trigger IEG expression required for long-term plasticity in the hippocampus.
Key words: IEG; place cell activity; medial septum; theta oscillations; hippocampus; FISH
Received Sept. 24, 2008;
revised Nov. 18, 2008;
accepted Dec. 3, 2008.
Correspondence should be addressed to John F. Guzowski, 108 Bonney Research Labs, Irvine, CA 92697-3800. Email: john.g{at}uci.edu
This article has been cited by other articles:

|
 |

|
 |
 
D. Panja, G. Dagyte, M. Bidinosti, K. Wibrand, A.-M. Kristiansen, N. Sonenberg, and C. R. Bramham
Novel Translational Control in Arc-dependent Long Term Potentiation Consolidation in Vivo
J. Biol. Chem.,
November 13, 2009;
284(46):
31498 - 31511.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. M. McKay, E. A. Matthews, F. A. Oliveira, and J. F. Disterhoft
Intrinsic Neuronal Excitability Is Reversibly Altered by a Single Experience in Fear Conditioning
J Neurophysiol,
November 1, 2009;
102(5):
2763 - 2770.
[Abstract]
[Full Text]
[PDF]
|
 |
|