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Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons

Nature Neuroscience volume 18, pages 11331142 (2015) | Download Citation

Abstract

Feature-selective firing allows networks to produce representations of the external and internal environments. Despite its importance, the mechanisms generating neuronal feature selectivity are incompletely understood. In many cortical microcircuits the integration of two functionally distinct inputs occurs nonlinearly through generation of active dendritic signals that drive burst firing and robust plasticity. To examine the role of this processing in feature selectivity, we recorded CA1 pyramidal neuron membrane potential and local field potential in mice running on a linear treadmill. We found that dendritic plateau potentials were produced by an interaction between properly timed input from entorhinal cortex and hippocampal CA3. These conjunctive signals positively modulated the firing of previously established place fields and rapidly induced new place field formation to produce feature selectivity in CA1 that is a function of both entorhinal cortex and CA3 input. Such selectivity could allow mixed network level representations that support context-dependent spatial maps.

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Acknowledgements

We thank S. Royer, M. Karlsson, J. Osborne, J. Chen and S. Sawtelle for assistance in designing the experimental setup; J. Cohen and A. Lee for technical assistance; W.L. Sun for fiber etching; B. Shields and M. Copeland for histology; M. Lengyel, E. Pastalkova, Y. Wang and B. Lustig for discussions; and M. Mehta, J. Dudman, A. Lee and N. Spruston for comments on the manuscript. This work was supported by Howard Hughes Medical Institute and in part by RIKEN, Wako-shi Japan and the Howard Hughes Medical Institute to the Massachusetts Institute of Technology (S.T.).

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Affiliations

  1. Howard Hughes Medical Institute, Janelia Research Campus, Ashburn, Virginia, USA.

    • Katie C Bittner
    • , Christine Grienberger
    • , Sachin P Vaidya
    • , Aaron D Milstein
    • , John J Macklin
    •  & Jeffrey C Magee
  2. RIKEN-MIT Center for Neural Circuit Genetics at the Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Junghyup Suh
    •  & Susumu Tonegawa
  3. Howard Hughes Medical Institute at the Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Junghyup Suh
    •  & Susumu Tonegawa

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Contributions

K.C.B. and J.C.M. designed experiments; K.C.B. and C.G. performed in vivo recordings; S.P.V. and A.D.M. performed in vitro recordings; J.J.M. designed and built light probes; J.S. and S.T. designed and produced pOxr1 Cre mice; J.C.M., K.C.B. and C.G. analyzed data. J.C.M. and K.C.B. wrote the manuscript with input from all authors.

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The authors declare no competing financial interests.

Corresponding author

Correspondence to Jeffrey C Magee.

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https://doi.org/10.1038/nn.4062

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