What do grid cells contribute to place cell firing?

Highlights • It is commonly assumed that grid cell inputs generate hippocampal place fields, but recent empirical evidence brings this assumption into doubt.• We suggest that place fields are primarily determined by environmental sensory inputs.• Grid cells provide a complementary path integration input and large-scale spatial metric.• Place and grid cell representations interact to support accurate coding of large-scale space.

[1]  J. Knierim,et al.  Influence of boundary removal on the spatial representations of the medial entorhinal cortex , 2008, Hippocampus.

[2]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[3]  S. Cheng,et al.  The structure of networks that produce the transformation from grid cells to place cells , 2011, Neuroscience.

[4]  B. McNaughton,et al.  Spatial selectivity of unit activity in the hippocampal granular layer , 1993, Hippocampus.

[5]  Francesca Cacucci,et al.  The role of environmental boundaries in the ontogeny of the hippocampal neural code for space , 2013 .

[6]  Susumu Tonegawa,et al.  Transgenic Inhibition of Synaptic Transmission Reveals Role of CA3 Output in Hippocampal Learning , 2008, Science.

[7]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Jonathan D. Cohen,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006 .

[9]  J. O’Keefe,et al.  Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells , 2005, Hippocampus.

[10]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

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

[12]  P. Best,et al.  Place cells and silent cells in the hippocampus of freely-behaving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Simon M Stringer,et al.  Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning , 2006, Network.

[14]  E. Kandel,et al.  Mice Expressing Activated CaMKII Lack Low Frequency LTP and Do Not Form Stable Place Cells in the CA1 Region of the Hippocampus , 1996, Cell.

[15]  J. Taube.  The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[16]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

[17]  Francesca Sargolini,et al.  Independence of landmark and self-motion-guided navigation: a different role for grid cells , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[19]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[20]  L F Abbott,et al.  Modular Realignment of Entorhinal Grid Cell Activity as a Basis for Hippocampal Remapping , 2011, The Journal of Neuroscience.

[21]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[22]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[23]  Neil Burgess,et al.  Predictions derived from modelling the hippocampal role in navigation , 2000, Biological Cybernetics.

[24]  P. Best,et al.  Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex , 1980, Brain Research.

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

[26]  G. Buzsáki,et al.  Spike phase precession persists after transient intrahippocampal perturbation , 2005, Nature Neuroscience.

[27]  B Poucet,et al.  Place cells in the ventral hippocampus of rats , 1994, Neuroreport.

[28]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  John O'Keefe,et al.  Independent rate and temporal coding in hippocampal pyramidal cells , 2003, Nature.

[30]  Caswell Barry,et al.  From A to Z: a potential role for grid cells in spatial navigation , 2012, Neural systems & circuits.

[31]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Michael Recce,et al.  A model of hippocampal function , 1994, Neural Networks.

[33]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[34]  E. Bostock,et al.  Experience‐dependent modifications of hippocampal place cell firing , 1991, Hippocampus.

[35]  R. Nicoll,et al.  Brain-Derived Neurotrophic Factor ( BDNF ) Modulates Inhibitory , But Not Excitatory , Transmission in the CA 1 Region of the Hippocampus , 1998 .

[36]  Mark P. Brandon,et al.  Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning , 2011, Science.

[37]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[38]  J. Lisman,et al.  Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state , 1993, Nature.

[39]  Thomas J. Wills,et al.  Development of the Hippocampal Cognitive Map in Preweanling Rats , 2010, Science.

[40]  T. Hafting,et al.  Hippocampus-independent phase precession in entorhinal grid cells , 2008, Nature.

[41]  M. Moser,et al.  Representation of Geometric Borders in the Developing Rat , 2014, Neuron.

[42]  M. Moser,et al.  Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity , 2013, Science.

[43]  K. Jeffery,et al.  The Boundary Vector Cell Model of Place Cell Firing and Spatial Memory , 2006, Reviews in the neurosciences.

[44]  J. O’Keefe.  Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[45]  Stephen Grossberg,et al.  Grid cell hexagonal patterns formed by fast self‐organized learning within entorhinal cortex , 2012, Hippocampus.

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

[47]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

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

[49]  D. Bilkey,et al.  Excitotoxic lesions of the pre‐ and parasubiculum disrupt the place fields of hippocampal pyramidal cells , 2004, Hippocampus.

[50]  A. J. Hill.  First occurrence of hippocampal spatial firing in a new environment , 1978, Experimental Neurology.

[51]  J. O’Keefe,et al.  Modeling place fields in terms of the cortical inputs to the hippocampus , 2000, Hippocampus.

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

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

[54]  T. Babb,et al.  Demonstration of axonal projections of neurons in the rat hippocampus and subiculum by intracellular injection of HRP , 1983, Brain Research.

[55]  M. Hasselmo.  A model of episodic memory: Mental time travel along encoded trajectories using grid cells , 2009, Neurobiology of Learning and Memory.

[56]  James J Knierim,et al.  Conflicts between Local and Global Spatial Frameworks Dissociate Neural Representations of the Lateral and Medial Entorhinal Cortex , 2013, The Journal of Neuroscience.

[57]  J. O’Keefe,et al.  An oscillatory interference model of grid cell firing , 2007, Hippocampus.

[58]  Menno P. Witter,et al.  Place Cells and Place Recognition Maintained by Direct Entorhinal-Hippocampal Circuitry , 2002, Science.

[59]  G. Buzsáki,et al.  Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop , 2009, Neuron.

[60]  Tom Hartley,et al.  What can the hippocampal representation of environmental geometry tell us about Hebbian learning? , 2002, Biological Cybernetics.

[61]  J. O’Keefe.  A review of the hippocampal place cells , 1979, Progress in Neurobiology.

[62]  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.

[63]  J. O’Keefe,et al.  Single unit activity in the rat hippocampus during a spatial memory task , 2004, Experimental Brain Research.

[64]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[65]  Mark C. Fuhs,et al.  A Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex , 2006, The Journal of Neuroscience.

[66]  Uğur M Erdem,et al.  A goal‐directed spatial navigation model using forward trajectory planning based on grid cells , 2012, The European journal of neuroscience.

[67]  Lucien T. Thompson,et al.  Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats , 1990, Brain Research.

[68]  Ila Fiete,et al.  Grid cells generate an analog error-correcting code for singularly precise neural computation , 2011, Nature Neuroscience.

[69]  T. Bliss,et al.  The Hippocampus Book , 2006 .

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

[71]  Robert D. Blitzer,et al.  Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus , 1990, Neuroscience Letters.

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

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

[74]  B. McNaughton,et al.  Place cells, head direction cells, and the learning of landmark stability , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  N. Burgess.  Grid cells and theta as oscillatory interference: Theory and predictions , 2008, Hippocampus.

[76]  David N. Lyttle,et al.  Spatial scale and place field stability in a grid‐to‐place cell model of the dorsoventral axis of the hippocampus , 2013, Hippocampus.

[77]  C. Barry,et al.  Learning in a geometric model of place cell firing , 2007, Hippocampus.

[78]  Francesco Savelli,et al.  Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. , 2010, Journal of neurophysiology.

[79]  P. Dudchenko.  The hippocampus as a cognitive map , 2010 .

[80]  E. Save,et al.  Unstable CA1 place cell representation in rats with entorhinal cortex lesions , 2008, The European journal of neuroscience.

[81]  L. Frank,et al.  Behavioral/Systems/Cognitive Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments , 2022 .

[82]  J. O’Keefe,et al.  Neural Representations of Location Composed of Spatially Periodic Bands , 2012, Science.

[83]  E. Save,et al.  Contribution of multiple sensory information to place field stability in hippocampal place cells , 2000, Hippocampus.

[84]  Kathryn J Jeffery,et al.  Heterogeneous Modulation of Place Cell Firing by Changes in Context , 2003, The Journal of Neuroscience.

[85]  Charlotte N. Boccara,et al.  Grid cells in pre- and parasubiculum , 2010, Nature Neuroscience.

[86]  K. Jeffery,et al.  How heterogeneous place cell responding arises from homogeneous grids—A contextual gating hypothesis , 2008, Hippocampus.

[87]  May-Britt Moser,et al.  The entorhinal grid map is discretized , 2012, Nature.

[88]  D. Touretzky,et al.  Cognitive maps beyond the hippocampus , 1997, Hippocampus.

[89]  Colin Molter,et al.  Impact of temporal coding of presynaptic entorhinal cortex grid cells on the formation of hippocampal place fields , 2008, Neural Networks.

[90]  H. Eichenbaum,et al.  Cues that hippocampal place cells encode: Dynamic and hierarchical representation of local and distal stimuli , 1997, Hippocampus.

[91]  John A. King,et al.  How vision and movement combine in the hippocampal place code , 2012, Proceedings of the National Academy of Sciences.

[92]  G. Einevoll,et al.  From grid cells to place cells: A mathematical model , 2006, Hippocampus.

[93]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

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

[95]  Sachin S. Deshmukh,et al.  Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[96]  Benjamin A. Dunn,et al.  Grid cells require excitatory drive from the hippocampus , 2013, Nature Neuroscience.

[97]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[98]  C. Barnes,et al.  Spatial Representation along the Proximodistal Axis of CA1 , 2010, Neuron.

[99]  K. Jeffery,et al.  Experience-dependent rescaling of entorhinal grids , 2007, Nature Neuroscience.

[100]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[101]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[102]  David J. Foster,et al.  A model of hippocampally dependent navigation, using the temporal difference learning rule , 2000, Hippocampus.

[103]  William W Lytton,et al.  Unmasking the CA1 Ensemble Place Code by Exposures to Small and Large Environments: More Place Cells and Multiple, Irregularly Arranged, and Expanded Place Fields in the Larger Space , 2008, The Journal of Neuroscience.

[104]  Natalie L. M. Cappaert,et al.  The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network , 2009, Nature Reviews Neuroscience.

[105]  Alessandro Treves,et al.  The role of competitive learning in the generation of DG fields from EC inputs , 2009, Cognitive Neurodynamics.

[106]  M. Moser,et al.  Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex , 2008, Neuron.

[107]  T. Hafting,et al.  Finite Scale of Spatial Representation in the Hippocampus , 2008, Science.

[108]  Doyun Lee,et al.  Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior , 2012, Science.

[109]  H. T. Blair,et al.  Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference , 2011, The Journal of Neuroscience.

[110]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.

[111]  J. O’Keefe,et al.  Grid cell firing patterns signal environmental novelty by expansion , 2012, Proceedings of the National Academy of Sciences.

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

[113]  Neil Burgess,et al.  Models of place and grid cell firing and theta rhythmicity , 2011, Current Opinion in Neurobiology.

[114]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[115]  J. Lisman,et al.  The Input–Output Transformation of the Hippocampal Granule Cells: From Grid Cells to Place Fields , 2009, The Journal of Neuroscience.

[116]  Sachin S. Deshmukh,et al.  Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex , 2011, Front. Behav. Neurosci..

[117]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[118]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .