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Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex

Nature Neuroscience volume 16, pages 1085–1093 (2013)Cite this article

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Abstract

In the hippocampus, spatial and non-spatial parameters may be represented by a dual coding scheme, in which coordinates in space are expressed by the collective firing locations of place cells and the diversity of experience at these locations is encoded by orthogonal variations in firing rates. Although the spatial signal may reflect input from medial entorhinal cortex, the sources of the variations in firing rate have not been identified. We found that rate variations in rat CA3 place cells depended on inputs from the lateral entorhinal cortex (LEC). Hippocampal rate remapping, induced by changing the shape or the color configuration of the environment, was impaired by lesions in those parts of the ipsilateral LEC that provided the densest input to the hippocampal recording position. Rate remapping was not observed in LEC itself. The findings suggest that LEC inputs are important for efficient rate coding in the hippocampus.

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Figure 1: Neurotoxic damage in the LEC, recording positions in the hippocampus and their connectional relationships.
Figure 2: Example rate maps showing that LEC lesions abolish rate remapping in response to a change in the shape of the recording enclosure.
Figure 3: Average data showing impaired hippocampal rate remapping in LEC-lesioned rats.
Figure 4: Rate remapping depends on the location of the lesion in LEC.
Figure 5: LEC lesions impair progressive rate remapping during morphing of square and circular environments.
Figure 6: LEC lesions disrupt rate remapping between black and white versions of the same box.
Figure 7: Average data for the black-white task.
Figure 8: Lack of rate remapping in LEC neurons.

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Acknowledgements

We thank A.M. Amundgård, K. Haugen, K. Jenssen, E. Kråkvik, R. Skjerpeng and H. Waade for technical assistance. This work was supported by the Kavli Foundation and a Centre of Excellence grant from the Research Council of Norway.

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  1. Li Lu and Jill K Leutgeb: These authors contributed equally to this work.

Authors and Affiliations

  1. Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim, Norway

    Li Lu, Jill K Leutgeb, Albert Tsao, Espen J Henriksen, Stefan Leutgeb, Carol A Barnes, Menno P Witter, May-Britt Moser & Edvard I Moser

  2. Division of Biological Sciences, Neurobiology Section and Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, California, USA

    Jill K Leutgeb & Stefan Leutgeb

  3. Division of Neural Systems, Evelyn F. McKnight Brain Institute, Memory and Aging, University of Arizona, Tucson, Arizona, USA

    Carol A Barnes

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Contributions

J.K.L., S.L., E.I.M. and M.-B.M. conceived and designed the experiment. E.J.H. made lesions. S.L., L.L. and E.J.H. implanted hippocampal tetrodes. J.K.L., L.L. and E.J.H. performed the hippocampal recording experiments. J.K.L., L.L. and S.L. analyzed the hippocampal data. A.T. implanted LEC tetrodes and recorded and analyzed LEC cells. L.L. made figures. L.L., E.J.H. and M.P.W. evaluated lesions and made unfolded maps. A.T., E.J.H., L.L. and M.P.W. determined LEC recording locations. M.P.W. carried out tracing experiments and analyses. E.I.M. and L.L. wrote the manuscript. M.-B.M. and E.I.M. supervised and coordinated the project. All of the authors contributed to discussion and interpretation.

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Correspondence to Li Lu, Jill K Leutgeb or Edvard I Moser.

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Lu, L., Leutgeb, J., Tsao, A. et al. Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16, 1085–1093 (2013). https://doi.org/10.1038/nn.3462

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