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Hippocampal Projections to the Ventral Striatum: From Spatial Memory to Motivated Behavior

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Space,Time and Memory in the Hippocampal Formation

Abstract

Multiple regions of the hippocampal formation project to the ventral striatum, a central node in brain circuits that subserve aspects of motivation. These projections emphasize information flow from the ventral (temporal) pole of the hippocampus and interact with converging projections and neuromodulatory inputs upon arrival in the ventral striatum. Simultaneous neural recordings in the rat show that ventral striatal activity displays intricate timing relationships with the hippocampus, spanning multiple timescales and behavioral states, such as theta phase precession during reward approach and reactivation of place-reward associations during sleep. Disconnection of the hippocampus and ventral striatum results in impairments in the use of spatial information for place preference, as well as in location-appropriate responding to reward-predictive cues. Together, these findings indicate that spatial and contextual information from the hippocampus shapes reward-predictive activity in the ventral striatum, which in turn contributes to the learning and expression of place-reward associations.

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Notes

  1. 1.

    Following convention, we take this term to include the dentate gyrus, the “CA” subfields of Ammon’s horn, and the subiculum.

  2. 2.

    Following Heimer et al. (1997) and others (Voorn et al. 2004; Haber 2009), we define the ventral striatum as the nucleus accumbens core, shell, and the striatal bridges of the olfactory tubercule, while recognizing that boundaries with the ventral caudate-putamen may not be sharp.

  3. 3.

    We note that the extent to which dorsal CA1 place cells show reward-related organization is an issue of long-standing debate. For instance, Hollup et al. (2001) found increased place cell density near reward sites, but this effect does not always manifest (e.g., Lansink et al. 2009; Van der Meer et al. 2010). This debate would benefit greatly from a single study identifying the conditions under which such effects are present and absent.

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Acknowledgments

We thank Tobias Bast for discussion. This work was supported by the Netherlands Organization for Scientific Research (VENI 863.10.013 to MvdM and 863.11.010 to C.S.L., VICI 918.46.609 to C.M.A.P.) and the National Science and Engineering Research Council (Canada, R.I. and MvdM).

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Authors and Affiliations

  1. Department of Biology and Centre for Theoretical Neuroscience, University of Waterloo, 200 University Ave W, Waterloo, ON, Canada, N2L 3G1

    Matthijs A. A. van der Meer

  2. Department of Psychology, University of Toronto at Scarborough, Toronto, ON, Canada

    Rutsuko Ito

  3. Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands

    Carien S. Lansink & Cyriel M. A. Pennartz

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  1. Matthijs A. A. van der Meer
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  2. Rutsuko Ito
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  3. Carien S. Lansink
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  4. Cyriel M. A. Pennartz
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Correspondence to Matthijs A. A. van der Meer .

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Editors and Affiliations

  1. Rappaport Faculty of Medicine, Technion- Israel Institute of Technology, Haifa, Israel

    Dori Derdikman

  2. The Solomon H. Snyder Dept. of Neurosc., John Hopkins University The Zanvyl Krieger Mind/Brain Institute, Baltimore, Maryland, USA

    James J. Knierim

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van der Meer, M.A.A., Ito, R., Lansink, C.S., Pennartz, C.M.A. (2014). Hippocampal Projections to the Ventral Striatum: From Spatial Memory to Motivated Behavior. In: Derdikman, D., Knierim, J. (eds) Space,Time and Memory in the Hippocampal Formation. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1292-2_18

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