Bayesian Integration of Information in Hippocampal Place Cells

Accurate spatial localization requires a mechanism that corrects for errors, which might arise from inaccurate sensory information or neuronal noise. In this paper, we propose that Hippocampal place cells might implement such an error correction mechanism by integrating different sources of information in an approximately Bayes-optimal fashion. We compare the predictions of our model with physiological data from rats. Our results suggest that useful predictions regarding the firing fields of place cells can be made based on a single underlying principle, Bayesian cue integration, and that such predictions are possible using a remarkably small number of model parameters.

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

[2]  K. Jeffery.  Self-localization and the entorhinal–hippocampal system , 2007, Current Opinion in Neurobiology.

[3]  Aapo Hyvärinen,et al.  Interpreting Neural Response Variability as Monte Carlo Sampling of the Posterior , 2002, NIPS.

[4]  A. Wohlgemuth.  5. Weber's Law in the Discrimination of Maze Distance by the White Rat. Yoshioka, J. G. , 1931 .

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

[6]  D. Tank,et al.  Intracellular dynamics of hippocampal place cells during virtual navigation , 2009, Nature.

[7]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

[8]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[9]  Romain Brette,et al.  Sensitivity of Noisy Neurons to Coincident Inputs , 2011, The Journal of Neuroscience.

[10]  Robert Trappl,et al.  Correction: Bayesian Integration of Information in Hippocampal Place Cells , 2015, PloS one.

[11]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[12]  Mark A. Pitt,et al.  Model Evaluation, Testing and Selection , 2005 .

[13]  Raluca Irina Odobescu.  EXTEROCEPTIVE AND INTEROCEPTIVE CUE CONTROL OF HIPPOCAMPAL PLACE CELLS , 2010 .

[14]  Eero P. Simoncelli,et al.  Noise characteristics and prior expectations in human visual speed perception , 2006, Nature Neuroscience.

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

[16]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[17]  A. Alonso,et al.  Oscillatory Activity in Entorhinal Neurons and Circuits: Mechanisms and Function , 2000, Annals of the New York Academy of Sciences.

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

[19]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

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

[21]  M. Witter,et al.  What Does the Anatomical Organization of the Entorhinal Cortex Tell Us? , 2008, Neural plasticity.

[22]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[23]  Mohammad Wahid Ansari,et al.  The legal status of in vitro embryos , 2014 .

[24]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  H. Gurden,et al.  Alteration of sensory-evoked metabolic and oscillatory activities in the olfactory bulb of GLAST-deficient mice , 2012, Front. Neural Circuits.

[26]  Matteo Colombo,et al.  Bayes in the Brain—On Bayesian Modelling in Neuroscience , 2012, The British Journal for the Philosophy of Science.

[27]  A D Redish,et al.  Prediction, sequences and the hippocampus , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  A S Etienne,et al.  Path integration in mammals and its interaction with visual landmarks. , 1996, The Journal of experimental biology.

[29]  Hugh F. Durrant-Whyte,et al.  Simultaneous localization and mapping: part I , 2006, IEEE Robotics & Automation Magazine.

[30]  Riichi Kajiwara,et al.  Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1—An anatomical study in the rat , 2008, Hippocampus.

[31]  M. de Curtis,et al.  Enhancement of temporal and spatial synchronization of entorhinal gamma activity by phase reset , 2002, Hippocampus.

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

[33]  R. Douglas,et al.  Behavioral assessment of visual acuity in mice and rats , 2000, Vision Research.

[34]  Tony J. Prescott,et al.  Hippocampus as unitary coherent particle filter , 2010, The 2010 International Joint Conference on Neural Networks (IJCNN).

[35]  Rajesh P. N. Rao.  Bayesian Computation in Recurrent Neural Circuits , 2004, Neural Computation.

[36]  Sang Ah Lee,et al.  Navigation as a source of geometric knowledge: Young children’s use of length, angle, distance, and direction in a reorientation task , 2012, Cognition.

[37]  M. Hasselmo.  Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting , 2008, Hippocampus.

[38]  G. Pfuhl,et al.  Precision and Reliability in Animal Navigation , 2011, Bulletin of mathematical biology.

[39]  Pete R. Jones,et al.  Development of Cue Integration in Human Navigation , 2008, Current Biology.

[40]  Rudy R. Negenborn,et al.  Robot Localization and Kalman Filters , 2003 .

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

[42]  J. G. Yoshioka,et al.  Weber's law in the discrimination of maze distance by the white rat , 1929 .

[43]  Menno Witter.  Entorhinal cortex , 2011, Scholarpedia.

[44]  Wolfgang Maass,et al.  Neural Dynamics as Sampling: A Model for Stochastic Computation in Recurrent Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

[45]  Jason B. Mattingley,et al.  Medial Parietal Cortex Encodes Perceived Heading Direction in Humans , 2010, The Journal of Neuroscience.

[46]  Omar J. Ahmed,et al.  The hippocampal rate code: anatomy, physiology and theory , 2009, Trends in Neurosciences.

[47]  Karl M Newell,et al.  The movement speed-accuracy relation in space-time. , 2013, Human movement science.

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

[49]  H. Eichenbaum,et al.  Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  Sophie Denève,et al.  Bayesian Spiking Neurons I: Inference , 2008, Neural Computation.

[51]  Romain Brette,et al.  Computing with Neural Synchrony , 2012, PLoS Comput. Biol..

[52]  M. Fyhn,et al.  Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex , 2008, Hippocampus.

[53]  Yasutaka Fujimoto,et al.  Grid-based localization and mapping method without odometry information , 2011, IECON 2011 - 37th Annual Conference of the IEEE Industrial Electronics Society.

[54]  Mark C. W. van Rossum,et al.  Accurate multiplication with noisy spiking neurons , 2011, Journal of neural engineering.

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

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

[57]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Dora E Angelaki,et al.  Computational approaches to spatial orientation: from transfer functions to dynamic Bayesian inference. , 2008, Journal of neurophysiology.

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

[60]  M. Gallagher,et al.  Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[61]  P. Berkes,et al.  Statistically Optimal Perception and Learning: from Behavior to Neural Representations , 2022 .

[62]  Daniela Montaldi,et al.  The role of recollection and familiarity in the functional differentiation of the medial temporal lobes , 2010, Hippocampus.

[63]  N. Burgess.  Spatial Cognition and the Brain , 2008, Annals of the New York Academy of Sciences.

[64]  David Ball,et al.  Maintaining a Cognitive Map in Darkness: The Need to Fuse Boundary Knowledge with Path Integration , 2012, PLoS Comput. Biol..

[65]  D. Amaral,et al.  Neurons, numbers and the hippocampal network. , 1990, Progress in brain research.

[66]  A. Azzalini.  The Skew‐normal Distribution and Related Multivariate Families * , 2005 .

[67]  Michael E. Hasselmo,et al.  Coincidence Detection of Place and Temporal Context in a Network Model of Spiking Hippocampal Neurons , 2007, PLoS Comput. Biol..

[68]  Alexandre Pouget,et al.  Optimal Sensorimotor Integration in Recurrent Cortical Networks: A Neural Implementation of Kalman Filters , 2007, The Journal of Neuroscience.

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

[70]  Nicholas T. Carnevale,et al.  Simulation of networks of spiking neurons: A review of tools and strategies , 2006, Journal of Computational Neuroscience.

[71]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[72]  P. Somogyi,et al.  Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro , 1996, Hippocampus.

[73]  N. Burgess,et al.  The hippocampus and memory: insights from spatial processing , 2008, Nature Reviews Neuroscience.

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

[75]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

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

[77]  Michael N. Shadlen,et al.  Probabilistic reasoning by neurons , 2007, Nature.

[78]  Tai Sing Lee,et al.  Hierarchical Bayesian inference in the visual cortex. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[79]  B. McNaughton,et al.  Self‐motion and the origin of differential spatial scaling along the septo‐temporal axis of the hippocampus , 2005, Hippocampus.

[80]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

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

[82]  Eric A. Zilli,et al.  Models of Grid Cell Spatial Firing Published 2005–2011 , 2012, Front. Neural Circuits.

[83]  Tatiana A. Engel,et al.  Subthreshold membrane-potential resonances shape spike-train patterns in the entorhinal cortex. , 2008, Journal of neurophysiology.

[84]  J. Rieser,et al.  Bayesian integration of spatial information. , 2007, Psychological bulletin.

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

[86]  Romain Brette,et al.  The Brian Simulator , 2009, Front. Neurosci..

[87]  Alexandre Pouget,et al.  Probabilistic Interpretation of Population Codes , 1996, Neural Computation.

[88]  N. Spruston,et al.  Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons , 2005, Nature Neuroscience.

[89]  J. Magee,et al.  Pathway Interactions and Synaptic Plasticity in the Dendritic Tuft Regions of CA1 Pyramidal Neurons , 2009, Neuron.

[90]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

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

[92]  B. McNaughton,et al.  Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input , 1994, Hippocampus.

[93]  Wei Ji Ma,et al.  Spiking networks for Bayesian inference and choice , 2008, Current Opinion in Neurobiology.

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

[95]  I. J. Myung,et al.  Applying Occam’s razor in modeling cognition: A Bayesian approach , 1997 .

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

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

[98]  Christof Koch,et al.  The role of single neurons in information processing , 2000, Nature Neuroscience.

[99]  Daniel M Wolpert,et al.  Bayesian integration in force estimation. , 2004, Journal of neurophysiology.

[100]  Szabolcs Káli,et al.  Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h-current and passive membrane characteristics , 2010, The Journal of physiology.

[101]  Tamás Kiss,et al.  Robust path integration in the entorhinal grid cell system with hippocampal feed-back , 2009, Biological Cybernetics.

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