Dynamic Control of Hippocampal Spatial Coding Resolution by Local Visual Cues

Animals can flexibly navigate in their environment. This ability is thought to rely on an internal cognitive map. An open question concerns the influence of local sensory cues on the cognitive map and notably their putative contribution to setting its spatial resolution. Here we compared the firing of hippocampal principal cells in mice navigating virtual reality environments in the presence or absence of local visual cues (virtual 3D objects). Objects improved the spatial representation both quantitatively (higher proportion of place cells) and qualitatively (smaller place fields with increased spatial selectivity and stability). This gain in spatial coding resolution was more pronounced near the objects and could be rapidly tuned by their manipulations. In addition, place cells displayed improved theta phase precession in the presence of objects. Thus the hippocampal mapping system can dynamically adjust its spatial coding resolution to local sensory cues available in the environment.

[1]  Sachin S. Deshmukh,et al.  Influence of local objects on hippocampal representations: Landmark vectors and memory , 2013, Hippocampus.

[2]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[3]  J. Knierim,et al.  Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. , 2011, Physiological reviews.

[4]  Mayank R Mehta,et al.  Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality , 2014, Nature Neuroscience.

[5]  Jadin C. Jackson,et al.  Network dynamics of hippocampal cell‐assemblies resemble multiple spatial maps within single tasks , 2007, Hippocampus.

[6]  Richard Kempter,et al.  Single-Trial Phase Precession in the Hippocampus , 2009, The Journal of Neuroscience.

[7]  E. Tolman.  Cognitive maps in rats and men. , 1948, Psychological review.

[8]  Bryan C. Souza,et al.  On Information Metrics for Spatial Coding , 2017, Neuroscience.

[9]  Matthew L. Shapiro,et al.  Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. , 1997 .

[10]  E. Save,et al.  Flexible use of proximal objects and distal cues by hippocampal place cells , 2007, Hippocampus.

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

[12]  Frances S. Chance,et al.  Erratum: Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex , 2013, Nature Neuroscience.

[13]  F. Battaglia,et al.  Single-Trial Properties of Place Cells in Control and CA1 NMDA Receptor Subunit 1-KO Mice , 2014, The Journal of Neuroscience.

[14]  Kenneth D Harris,et al.  Spike sorting for large, dense electrode arrays , 2015, Nature Neuroscience.

[15]  J. O’Neill,et al.  The reorganization and reactivation of hippocampal maps predict spatial memory performance , 2010, Nature Neuroscience.

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

[17]  Dmitriy Aronov,et al.  Engagement of Neural Circuits Underlying 2D Spatial Navigation in a Rodent Virtual Reality System , 2014, Neuron.

[18]  Albert K. Lee,et al.  Large environments reveal the statistical structure governing hippocampal representations , 2014, Science.

[19]  G. Buzsáki,et al.  Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies , 2006, Neuron.

[20]  Attila Losonczy,et al.  Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1 , 2016, Neuron.

[21]  C. Petersen,et al.  Reward-Based Learning Drives Rapid Sensory Signals in Medial Prefrontal Cortex and Dorsal Hippocampus Necessary for Goal-Directed Behavior , 2018, Neuron.

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

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

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

[25]  Sébastien Royer,et al.  Place cells are more strongly tied to landmarks in deep than in superficial CA1 , 2017, Nature Communications.

[26]  Andrew P Maurer,et al.  The influence of objects on place field expression and size in distal hippocampal CA1 , 2011, Hippocampus.

[27]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity , 1989 .

[28]  B. Strowbridge,et al.  Visual landmarks facilitate rodent spatial navigation in virtual reality environments. , 2012, Learning & memory.

[29]  James J Knierim,et al.  Integration of objects and space in perception and memory , 2017, Nature Neuroscience.

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

[31]  Russell A. Epstein,et al.  The cognitive map in humans: spatial navigation and beyond , 2017, Nature Neuroscience.

[32]  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.

[33]  Ricardo Chavarriaga,et al.  Robust self-localisation and navigation based on hippocampal place cells , 2005, Neural Networks.

[34]  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.

[35]  B L McNaughton,et al.  Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. , 1998, Journal of neurophysiology.

[36]  E. Kandel,et al.  Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory , 2004, Neuron.

[37]  W. Gerstner,et al.  Is there a geometric module for spatial orientation? Insights from a rodent navigation model. , 2009, Psychological review.

[38]  E N Brown,et al.  A Statistical Paradigm for Neural Spike Train Decoding Applied to Position Prediction from Ensemble Firing Patterns of Rat Hippocampal Place Cells , 1998, The Journal of Neuroscience.

[39]  Adam Johnson,et al.  Triple Dissociation of Information Processing in Dorsal Striatum, Ventral Striatum, and Hippocampus on a Learned Spatial Decision Task , 2010, Neuron.

[40]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[43]  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.

[44]  Richard Kempter,et al.  Quantifying circular–linear associations: Hippocampal phase precession , 2012, Journal of Neuroscience Methods.

[45]  Nachum Ulanovsky,et al.  Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation , 2015, Nature Reviews Neuroscience.

[46]  M. Häusser,et al.  Cellular mechanisms of spatial navigation in the medial entorhinal cortex , 2013, Nature Neuroscience.

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

[48]  K. D. Taylor.  Range of Movement and Activity of Common Rats (Rattus norvegicus) on Agricultural Land , 1978 .

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

[50]  David S. Lorberbaum,et al.  Genetic evidence that Nkx2.2 acts primarily downstream of Neurog3 in pancreatic endocrine lineage development , 2017, eLife.

[51]  Tomoki Fukai,et al.  Dynamic embedding of salience coding in hippocampal spatial maps , 2018, bioRxiv.

[52]  György Buzsáki,et al.  Alteration of Theta Timescale Dynamics of Hippocampal Place Cells by a Cannabinoid Is Associated with Memory Impairment , 2009, The Journal of Neuroscience.

[53]  James J Knierim,et al.  Distal landmarks and hippocampal place cells: Effects of relative translation versus rotation , 2003, Hippocampus.

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

[55]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[56]  Jeremy D. Cohen,et al.  Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments , 2017, eLife.

[57]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[58]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[59]  A Schnee,et al.  Rats are able to navigate in virtual environments , 2005, Journal of Experimental Biology.

[60]  Kempter Richard,et al.  Single-trial phase precession in the hippocampus , 2009 .

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

[62]  Hugo J. Spiers,et al.  Place Field Repetition and Purely Local Remapping in a Multicompartment Environment , 2013, Cerebral cortex.

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

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

[65]  B. McNaughton,et al.  Local Sensory Cues and Place Cell Directionality: Additional Evidence of Prospective Coding in the Hippocampus , 2004, The Journal of Neuroscience.

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

[67]  György Buzsáki,et al.  Hippocampal place cell assemblies are speed-controlled oscillators , 2007, Proceedings of the National Academy of Sciences.

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

[69]  J. Csicsvari,et al.  Firing rate and theta‐phase coding by hippocampal pyramidal neurons during ‘space clamping’ , 1999, The European journal of neuroscience.

[70]  Francesca Sargolini,et al.  Is there a pilot in the brain? Contribution of the self-positioning system to spatial navigation , 2015, Front. Behav. Neurosci..

[71]  S. Molden,et al.  Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task , 2001, The Journal of Neuroscience.

[72]  Steven J. Middleton,et al.  Silencing CA3 disrupts temporal coding in the CA1 ensemble , 2016, Nature Neuroscience.

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