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Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks

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Abstract

Hippocampal place cells are selectively active when a rat occupies restricted locations in an environment, and head direction cells fire selectively when the rat’s head is pointed in a particular direction in allocentric space. Both place cells and head direction cells are usually coupled, and they are controlled by a complex interaction between external landmarks and idiothetic cues. Most studies have investigated this interaction by rotating the landmarks in the environment. In contrast, a recent study translated the apparatus relative to the landmarks in an environment and found that most place cells maintained the same preferred location on the apparatus regardless of the location of the apparatus in the room. Because head direction cells are insensitive to the rat’s location in an environment, the distal landmarks may influence the place field firing locations primarily by controlling the bearing of the head direction cell system. To address this question, ensembles of CA1 place cells and head direction cells of the anterior thalamus were recorded simultaneously, as a rectangular or circular track was moved to different locations in a room with distinct visual landmarks. Most place cells maintained their firing fields relative to the track when the track was translated, and head direction cells maintained the same preferred firing direction. When the distal landmarks were rotated around the track, the firing fields of place cells and the preferred directions of head direction cells rotated with the cues. These results suggest that the precise firing locations of place cells are controlled by an interaction between local and idiothetic cues, and the orientation of the CA1 ensemble representation relative to the distal landmarks may be controlled indirectly by the distal landmarks’ influence over the bearing of the head direction cell system.

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Acknowledgements

We thank Dr. Inah Lee and Geeta Rao for assistance with data collection, analysis, and manuscript preparation. This work was supported by grants from the Public Health Service (R01 NS39456 and K02 MH63297) and by the Lucille P. Markey Charitable Trust.

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  1. Department of Neurobiology & Anatomy, W.M. Keck Center for the Neurobiology of Learning and Memory, University of Texas Medical School at Houston, P.O. Box 20708, Houston, TX 77225, USA

    D. Yoganarasimha & James J. Knierim

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  1. D. Yoganarasimha
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  2. James J. Knierim
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Correspondence to James J. Knierim.

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Yoganarasimha, D., Knierim, J.J. Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks. Exp Brain Res 160, 344–359 (2005). https://doi.org/10.1007/s00221-004-2016-9

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