Odor supported place cell model and goal navigation in rodents

Experiments with rodents demonstrate that visual cues play an important role in the control of hippocampal place cells and spatial navigation. Nevertheless, rats may also rely on auditory, olfactory and somatosensory stimuli for orientation. It is also known that rats can track odors or self-generated scent marks to find a food source. Here we model odor supported place cells by using a simple feed-forward network and analyze the impact of olfactory cues on place cell formation and spatial navigation. The obtained place cells are used to solve a goal navigation task by a novel mechanism based on self-marking by odor patches combined with a Q-learning algorithm. We also analyze the impact of place cell remapping on goal directed behavior when switching between two environments. We emphasize the importance of olfactory cues in place cell formation and show that the utility of environmental and self-generated olfactory cues, together with a mixed navigation strategy, improves goal directed navigation.

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

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

[3]  W. K. Honig,et al.  Spatial memory deficit in senescent rats. , 1980, Canadian journal of psychology.

[4]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[5]  A. J. Hill,et al.  Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat , 1981, Experimental Neurology.

[6]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[7]  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.

[8]  D. Eilam,et al.  Home base behavior of rats (Rattus norvegicus) exploring a novel environment , 1989, Behavioural Brain Research.

[9]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  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.

[11]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Patricia E. Sharp,et al.  Computer simulation of hippocampal place cells , 1991, Psychobiology.

[13]  W. T. Tomlinson,et al.  Hamsters remember spatial information derived from olfactory cues , 1991 .

[14]  M. Shapiro,et al.  A simple network model simulates hippocampal place fields: parametric analyses and physiological predictions. , 1993, Behavioral neuroscience.

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

[16]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[18]  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.

[19]  R. Andrew Russell,et al.  Laying and sensing odor markings as a strategy for assisting mobile robot navigation tasks , 1995, IEEE Robotics Autom. Mag..

[20]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  P. Lavenex,et al.  Influence of local environmental olfactory cues on place learning in rats , 1995, Physiology & Behavior.

[22]  P. E. Sharp,et al.  Simulation of spatial learning in the Morris water maze by a neural network model of the hippocampal formation and nucleus accumbens , 1995, Hippocampus.

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

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

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

[26]  Robert U Muller,et al.  Head direction cells: properties and functional significance , 1996, Current Opinion in Neurobiology.

[27]  P Lavenex,et al.  Integration of olfactory information in a spatial representation enabling accurate arm choice in the radial arm maze. , 1996, Learning & memory.

[28]  M. Recce,et al.  Memory for places: A navigational model in support of Marr's theory of hippocampal function , 1996, Hippocampus.

[29]  H. Eichenbaum,et al.  Discordance of spatial representation in ensembles of hippocampal place cells , 1997, Hippocampus.

[30]  O. Bousquet,et al.  Spatial Learning and Localization in Animals : A Computational Model and Its Implications for Mobile Robots , 1997 .

[31]  Charles W. Anderson,et al.  Comparison of CMACs and radial basis functions for local function approximators in reinforcement learning , 1997, Proceedings of International Conference on Neural Networks (ICNN'97).

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

[33]  N. Brunel,et al.  Plasticity of directional place fields in a model of rodent CA3 , 1998, Hippocampus.

[34]  B. McNaughton,et al.  Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. , 1998, Journal of neurophysiology.

[35]  O. Bousquet,et al.  Is the hippocampus a Kalman filter? , 1998, Pacific Symposium on Biocomputing. Pacific Symposium on Biocomputing.

[36]  P. Lavenex,et al.  Olfactory traces and spatial learning in rats , 1998, Animal Behaviour.

[37]  J. Prados,et al.  Locating an invisible goal in a water maze requires at least two landmarks , 1998, Psychobiology.

[38]  G. M. Martin,et al.  Open Field Motor Patterns and Object Marking, but Not Object Sniffing, Are Altered by Ibotenate Lesions of the Hippocampus , 1999, Neurobiology of Learning and Memory.

[39]  I. Whishaw,et al.  Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation , 1999, Behavioural Brain Research.

[40]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[41]  K. Jeffery,et al.  Learned interaction of visual and idiothetic cues in the control of place field orientation , 1999, Experimental Brain Research.

[42]  J. O’Keefe Do hippocampal pyramidal cells signal non‐spatial as well as spatial information? , 1999, Hippocampus.

[43]  Jun Nishii A Learning Model of a Periodic Locomotor Pattern by the Central Pattern Generator , 1999, Adapt. Behav..

[44]  Angelo Arleo,et al.  Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity , 2000, Biological Cybernetics.

[45]  M. Griebel,et al.  The modelling of odour dispersion with time-resolved models. , 2000 .

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

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

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

[49]  P. Dudchenko,et al.  How do animals actually solve the T maze? , 2001, Behavioral neuroscience.

[50]  I. Whishaw,et al.  Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests , 2001, Behavioural Brain Research.

[51]  I. Whishaw,et al.  Rats can track odors, other rats, and themselves: implications for the study of spatial behavior , 2002, Behavioural Brain Research.

[52]  Douglas G Wallace,et al.  Quantification of a single exploratory trip reveals hippocampal formation mediated dead reckoning , 2002, Journal of Neuroscience Methods.

[53]  Philippe Gaussier,et al.  From view cells and place cells to cognitive map learning: processing stages of the hippocampal system , 2002, Biological Cybernetics.

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

[55]  C. Hölscher Time, Space and Hippocampal Functions , 2003, Reviews in the neurosciences.

[56]  J. Taube,et al.  Behavioral/systems/cognitive Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network , 2022 .

[57]  Stefan Wermter,et al.  Learning Localisation Based on Landmarks Using Self-Organisation , 2003, ICANN.

[58]  K. Jeffery,et al.  Preserved performance in a hippocampal‐dependent spatial task despite complete place cell remapping , 2003, Hippocampus.

[59]  I. Whishaw,et al.  Odor tracking in rats with orbital frontal lesions. , 2003, Behavioral neuroscience.

[60]  Angelo Arleo,et al.  Cognitive navigation based on nonuniform Gabor space sampling, unsupervised growing networks, and reinforcement learning , 2004, IEEE Transactions on Neural Networks.

[61]  Andrew W. Moore,et al.  Locally Weighted Learning for Control , 1997, Artificial Intelligence Review.

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

[63]  J. Knierim,et al.  Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks , 2004, Experimental Brain Research.

[64]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 1983, Experimental Brain Research.

[65]  Ariane S Etienne,et al.  Path integration in mammals , 2004, Hippocampus.

[66]  Roland Maurer,et al.  Resetting the path integrator: a basic condition for route-based navigation , 2004, Journal of Experimental Biology.

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

[68]  Robert Ollington,et al.  Learning Place Cells from Sonar data , 2004 .

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

[70]  I. Whishaw,et al.  Home bases formed to visual cues but not to self‐movement (dead reckoning) cues in exploring hippocampectomized rats , 2005, The European journal of neuroscience.

[71]  Günther Palm,et al.  Biomimetic Neural Learning for Intelligent Robots - Intelligent Systems, Cognitive Robotics, and Neuroscience , 2005, Biomimetic Neural Learning for Intelligent Robots.

[72]  T. S. Collett,et al.  Landmark learning and visuo-spatial memories in gerbils , 1986, Journal of Comparative Physiology A.

[73]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[74]  Ricardo Chavarriaga,et al.  Spatial Representation and Navigation in a Bio-inspired Robot , 2005, Biomimetic Neural Learning for Intelligent Robots.

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

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

[77]  Roland Vollgraf,et al.  From grids to places , 2007, Journal of Computational Neuroscience.

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

[79]  András Lörincz,et al.  Independent component analysis forms place cells in realistic robot simulations , 2006, Neurocomputing.

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

[81]  I. Whishaw,et al.  The point of entry contributes to the organization of exploratory behavior of rats on an open field: An example of spontaneous episodic memory , 2007, Behavioural Brain Research.

[82]  Jeffrey L. Krichmar,et al.  Spatial navigation and causal analysis in a brain-based device modeling cortical-hippocampal interactions , 2007, Neuroinformatics.