Hippocampal Global Remapping Can Occur without Input from the Medial Entorhinal Cortex

SUMMARY The high storage capacity of the episodic memory system relies on distinct representations for events that are separated in time and space. The spatial component of these computations includes the formation of independent maps by hippocampal place cells across environments, referred to as global re-mapping. Such remapping is thought to emerge by the switching of input patterns from specialized spatially selective cells in medial entorhinal cortex (mEC), such as grid and border cells. Although it has been shown that acute manipulations of mEC firing patterns are sufficient for inducing hippocampal remapping, it remains unknown whether specialized spatial mEC inputs are necessary for the reorganization of hippocampal spatial representations. Here, we examined remapping in rats without mEC input to the hippocampus and found that highly distinct spatial maps emerged rapidly in every individual rat. Our data suggest that hippocampal spatial computations do not depend on inputs from specialized cell types in mEC.

[1]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

[2]  Sandro Romani,et al.  Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells , 2017, Nature Neuroscience.

[3]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[4]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[5]  Carol A Barnes,et al.  Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex , 2013, Nature Neuroscience.

[6]  Fraser T. Sparks,et al.  Neuronal code for extended time in the hippocampus , 2012, Proceedings of the National Academy of Sciences.

[7]  D S Touretzky,et al.  Theory of rodent navigation based on interacting representations of space , 1996, Hippocampus.

[8]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

[9]  Eric A. Zilli,et al.  Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior , 2005, Hippocampus.

[10]  Richard Kempter,et al.  Inheritance of Hippocampal Place Fields Through Hebbian Learning: Effects of Theta Modulation and Phase Precession on Structure Formation , 2015, Neural Computation.

[11]  Kechen Zhang,et al.  Sensory Feedback, Error Correction, and Remapping in a Multiple Oscillator Model of Place-Cell Activity , 2011, Front. Comput. Neurosci..

[12]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.

[13]  Nils Z. Borgesius,et al.  A Novel Mechanism for the Grid-to-Place Cell Transformation Revealed by Transgenic Depolarization of Medial Entorhinal Cortex Layer II , 2017, Neuron.

[14]  Brittney L. Boublil,et al.  Hippocampal activation during the recall of remote spatial memories in radial maze tasks , 2013, Neurobiology of Learning and Memory.

[15]  H. Eichenbaum,et al.  Complementary Functional Organization of Neuronal Activity Patterns in the Perirhinal, Lateral Entorhinal, and Medial Entorhinal Cortices , 2016, The Journal of Neuroscience.

[16]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[17]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

[18]  Jill K. Leutgeb,et al.  Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes , 2017, Neuron.

[19]  A. Treves,et al.  Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1 , 2004, Science.

[20]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

[21]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[22]  F. H. Lopes da Silva,et al.  Cortico‐hippocampal communication by way of parallel parahippocampal‐subicular pathways , 2000, Hippocampus.

[23]  Surya Ganguli,et al.  Cell types for our sense of location: where we are and where we are going , 2017, Nature Neuroscience.

[24]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas , 2007, Hippocampus.

[25]  R. Muller,et al.  Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli , 2000, The Journal of general physiology.

[26]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  K. Miyazaki,et al.  Different representation of forthcoming reward in nucleus accumbens and medial prefrontal cortex , 2004, Neuroreport.

[28]  Edward S Boyden,et al.  Transient optogenetic inactivation of the medial entorhinal cortex biases the active population of hippocampal neurons , 2016, Hippocampus.

[29]  Thomas J. Wills,et al.  Long-term plasticity in hippocampal place-cell representation of environmental geometry , 2002, Nature.

[30]  H. Yamahachi,et al.  Hippocampal Remapping after Partial Inactivation of the Medial Entorhinal Cortex , 2015, Neuron.

[31]  Jadin C. Jackson,et al.  Quantitative measures of cluster quality for use in extracellular recordings , 2005, Neuroscience.

[32]  Ashley N. Linder,et al.  The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations , 2011, Science.

[33]  M. Moser,et al.  Traces of Experience in the Lateral Entorhinal Cortex , 2013, Current Biology.

[34]  James L. McClelland,et al.  Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off , 1994, Hippocampus.

[35]  Mark P. Brandon,et al.  New and Distinct Hippocampal Place Codes Are Generated in a New Environment during Septal Inactivation , 2014, Neuron.

[36]  May-Britt Moser,et al.  From cortical modules to memories , 2014, Current Opinion in Neurobiology.

[37]  T. Bonhoeffer,et al.  Grid cells and cortical representation , 2014, Nature Reviews Neuroscience.

[38]  T. Südhof.  Reproducibility: Experimental mismatch in neural circuits , 2015, Nature.

[39]  C. Köhler.  Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex , 1985, The Journal of comparative neurology.

[40]  Chenglin Miao,et al.  Place cells in the hippocampus: Eleven maps for eleven rooms , 2014, Proceedings of the National Academy of Sciences.

[41]  Larry R Squire,et al.  Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. , 2014, Cell reports.

[42]  J. Knierim,et al.  Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3 , 2004, Nature.

[43]  Christian Leibold,et al.  Hippocampal Remapping Is Constrained by Sparseness rather than Capacity , 2014, PLoS Comput. Biol..

[44]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[45]  D. Durstewitz,et al.  Contextual encoding by ensembles of medial prefrontal cortex neurons , 2012, Proceedings of the National Academy of Sciences.

[46]  Mark P. Brandon,et al.  THE MEDIAL ENTORHINAL CORTEX IS NECESSARY FOR TEMPORAL ORGANIZATION OF HIPPOCAMPAL NEURONAL ACTIVITY , 2015, Nature Neuroscience.

[47]  F. H. Lopes da Silva,et al.  Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum , 2001, Hippocampus.

[48]  N. Tamamaki,et al.  Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats , 1995, The Journal of comparative neurology.

[49]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.