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The Journal of Neuroscience, February 4, 2009, 29(5):1381-1394; doi:10.1523/JNEUROSCI.4339-08.2009

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Behavioral/Systems/Cognitive
Behavior-Dependent Coordination of Multiple Theta Dipoles in the Hippocampus

Sean M. Montgomery, Martha I. Betancur, and György Buzsáki

Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey 07102

Correspondence should be addressed to György Buzsáki, Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark NJ 07102. Email: buzsaki{at}rutgers.edu

Theta (4–10 Hz) oscillations in the hippocampus are thought to be important for plasticity, temporal coding, learning, and memory. The hippocampal system has been postulated to have two (or more) rhythmic sources of theta oscillations, but little is known about the behavior-dependent interplay of theta oscillations in different subregions and layers of the hippocampus. We tested rats in a hippocampus-dependent delayed spatial alternation task on a modified T-maze while simultaneously recording local field potentials from dendritic and somatic layers of the dentate gyrus, CA3, and CA1 regions using high-density, 96-site silicon probes. We found that while theta oscillations were generally coherent throughout the hippocampus, the power, coherence, and phase of theta oscillations fluctuated in a layer-specific manner, confirming the presence of multiple interdependent dipoles. Layer-dependent changes in the power and coherence of theta oscillations varied with aspects of both the memory and control (non-mnemonic) tasks, but only a small fraction of the variance could be explained by running speed or acceleration. Furthermore, the phase lag between theta oscillations in the CA3 and CA1 pyramidal layers was significantly smaller on the maze arm approaching the T-junction than on other arms of the alternation task or on comparable segments of control tasks. Overall, our findings reveal a consortium of layer-specific theta dipoles (current sinks and sources) generated by the rhythmic flow of ions into and out of hippocampal cells. Moreover, our data suggest that these different theta generators flexibly coordinate hippocampal regions and layers to support behavioral task performance.

Key words: hippocampal function; theta rhythm; oscillator; CA1; CA3; dentate gyrus; memory; synchrony; network

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Received Aug. 28, 2008; revised Oct. 28, 2008; accepted Dec. 7, 2008.

Correspondence should be addressed to György Buzsáki, Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark NJ 07102. Email: buzsaki{at}rutgers.edu

Related articles in J. Neurosci.:

The Multiple Origins and Laminar Topography of the Hippocampal Theta Rhythm

Prasad Shirvalkar and Amir S. Bahar
J. Neurosci. 2009 29: 7111-7113. [Full Text]  

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				D. Robbe and G. Buzsaki Alteration of Theta Timescale Dynamics of Hippocampal Place Cells by a Cannabinoid Is Associated with Memory Impairment J. Neurosci., October 7, 2009; 29(40): 12597 - 12605. [Abstract] [Full Text] [PDF]

				P. Shirvalkar and A. S. Bahar The Multiple Origins and Laminar Topography of the Hippocampal Theta Rhythm J. Neurosci., June 3, 2009; 29(22): 7111 - 7113. [Full Text] [PDF]

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