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The Journal of Neuroscience, May 12, 2004, 24(19):4541-4550; doi:10.1523/JNEUROSCI.4896-03.2004

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Behavioral/Systems/Cognitive
Local Sensory Cues and Place Cell Directionality: Additional Evidence of Prospective Coding in the Hippocampus

Francesco P. Battaglia, Gary R. Sutherland, and Bruce L. McNaughton

Arizona Research Laboratories, Division of Neural Systems, Memory, and Aging, University of Arizona, Tucson, Arizona 85724-5115

In tasks involving goal-directed, stereotyped trajectories on uniform tracks, the spatially selective activity of hippocampal principal cells depends on the animal's direction of motion. Principal cell ensemble activity while the rat moves in opposite directions through a given location is typically uncorrelated. It is shown here, with data from three experiments, that multimodal, local sensory cues can change the directional properties of CA1 pyramidal cells, inducing bidirectionality in a significant proportion of place cells. For a majority of these bidirectional place cells, place field centers in the two directions of motion were displaced relative to one another, as would be the case if the cells were representing a position in space 5-10 cm ahead of the rat or if place cells were subject to strong accommodation or inhibition in the latter half of their input fields. However, place field density was not affected by the presence of local cues, but in the experimental condition with the most salient sensory cues, the CA1 population vectors in the "cue-rich" condition were sparser and changed more quickly in space than in the "cue-poor" condition. These results suggest that "view-invariant" object representations are projected to the hippocampus from lower cortical areas and can have the effect of increasing the correlation of the hippocampal input vectors in the two directions, hence decreasing the orthogonality of hippocampal output.

Key words: neural ensembles; CA1; in vivo unit recording; behavior; hippocampus; spatial; population coding; multiple single-unit recording; cognitive map

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Received Oct 31, 2003; revised March 25, 2004; accepted March 26, 2004.

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