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The Journal of Neuroscience, October 29, 2008, 28(44):11250-11262; doi:10.1523/JNEUROSCI.2862-08.2008

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Behavioral/Systems/Cognitive
Unmasking the CA1 Ensemble Place Code by Exposures to Small and Large Environments: More Place Cells and Multiple, Irregularly Arranged, and Expanded Place Fields in the Larger Space

André A. Fenton,^1,3 Hsin-Yi Kao,⁴ Samuel A. Neymotin,⁵ Andrey Olypher,⁶ Yevgeniy Vayntrub,¹ William W. Lytton,^1,2,3 and Nandor Ludvig⁷

Departments of ¹Physiology and Pharmacology, and ²Neurology, ³Robert F. Furchgott Center for Neuroscience, ⁴Graduate Program in Neural and Behavioral Science, and ⁵Graduate Program in Biomedical Engineering, State University of New York, Brooklyn, New York 11203, ⁶Biology Department, Emory University, Atlanta, Georgia 30322, and ⁷Department of Neurology, Comprehensive Epilepsy Center, New York University School of Medicine, New York, New York 10016

Correspondence should be addressed to either of the following: André A. Fenton at the above address, Email: afenton{at}downstate.edu; or Nandor Ludvig at the above address, E-mail: Email: nandor.ludvig{at}nyumc.org

In standard experimental environments, a constant proportion of CA1 principal cells are place cells, each with a spatial receptive field called a place field. Although the properties of place cells are a basis for understanding the mammalian representation of spatial knowledge, there is no consensus on which of the two fundamental neural-coding hypotheses correctly accounts for how place cells encode spatial information. Within the dedicated-coding hypothesis, the current activity of each cell is an independent estimate of the location with respect to its place field. The average of the location estimates from many cells represents current location, so a dedicated place code would degrade if single cells had multiple place fields. Within the alternative, ensemble-coding hypothesis, the concurrent discharge of many place cells is a vector that represents current location. An ensemble place code is not degraded if single cells have multiple place fields as long as the discharge vector at each location is unique. Place cells with multiple place fields might be required to represent the substantially larger space in more natural environments. To distinguish between the dedicated-coding and ensemble-coding hypotheses, we compared the characteristics of CA1 place fields in a standard cylinder and an approximately six times larger chamber. Compared with the cylinder, in the chamber, more CA1 neurons were place cells, each with multiple, irregularly arranged, and enlarged place fields. The results indicate that multiple place fields is a fundamental feature of CA1 place cell activity and that, consequently, an ensemble place code is required for CA1 discharge to accurately signal location.

Key words: hippocampus; place cells; neuronal ensembles; CA1; spatial cognition; hippocampal function; extracellular recording

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Received June 22, 2008; revised Sept. 10, 2008; accepted Sept. 18, 2008.

Correspondence should be addressed to either of the following: André A. Fenton at the above address, Email: afenton{at}downstate.edu; or Nandor Ludvig at the above address, E-mail: Email: nandor.ludvig{at}nyumc.org

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