Enhancement of Hippocampal Spatial Decoding Using a Dynamic Q-Learning Method With a Relative Reward Using Theta Phase Precession

Hippocampal place cells and interneurons in mammals have stable place fields and theta phase precession profiles that encode spatial environmental information. Hippocampal CA1 neurons can represent the animal's location and prospective information about the goal location. Reinforcement learning (RL) algorithms such as Q-learning have been used to build the navigation models. However, the traditional Q-learning ([Formula: see text]Q-learning) limits the reward function once the animals arrive at the goal location, leading to unsatisfactory location accuracy and convergence rates. Therefore, we proposed a revised version of the Q-learning algorithm, dynamical Q-learning ([Formula: see text]Q-learning), which assigns the reward function adaptively to improve the decoding performance. Firing rate was the input of the neural network of [Formula: see text]Q-learning and was used to predict the movement direction. On the other hand, phase precession was the input of the reward function to update the weights of [Formula: see text]Q-learning. Trajectory predictions using [Formula: see text]Q- and [Formula: see text]Q-learning were compared by the root mean squared error (RMSE) between the actual and predicted rat trajectories. Using [Formula: see text]Q-learning, significantly higher prediction accuracy and faster convergence rate were obtained compared with [Formula: see text]Q-learning in all cell types. Moreover, combining place cells and interneurons with theta phase precession improved the convergence rate and prediction accuracy. The proposed [Formula: see text]Q-learning algorithm is a quick and more accurate method to perform trajectory reconstruction and prediction.

[1]  F. Jaw,et al.  Central Thalamic Deep-Brain Stimulation Alters Striatal-Thalamic Connectivity in Cognitive Neural Behavior , 2016, Front. Neural Circuits.

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

[3]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[4]  Roddy M. Grieves,et al.  Place cells on a maze encode routes rather than destinations , 2016, eLife.

[5]  Douglas A Nitz,et al.  Discrete place fields of hippocampal formation interneurons. , 2007, Journal of neurophysiology.

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

[7]  R. Reilly,et al.  Extrafield Activity Shifts the Place Field Center of Mass to Encode Aversive Experience , 2019, eNeuro.

[8]  Andrew M. Wikenheiser,et al.  Hippocampal theta sequences reflect current goals , 2015, Nature Neuroscience.

[9]  Manuel Graña,et al.  Concurrent Modular Q-Learning with Local Rewards on Linked Multi-Component Robotic Systems , 2011, IWINAC.

[10]  Chantal E. Stern,et al.  Theta rhythm and the encoding and retrieval of space and time , 2014, NeuroImage.

[11]  Ron Meir,et al.  Extracting grid cell characteristics from place cell inputs using non-negative principal component analysis , 2016, eLife.

[12]  Ulric J. Lund Least circular distance regression for directional data , 1999 .

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

[14]  Adriano B. L. Tort,et al.  Reactivation of time cell sequences in the hippocampus , 2018, bioRxiv.

[15]  Jadin C. Jackson,et al.  Reward Expectancy Strengthens CA1 Theta and Beta Band Synchronization and Hippocampal-Ventral Striatal Coupling , 2016, The Journal of Neuroscience.

[16]  Roddy M. Grieves,et al.  The representation of space in the brain , 2017, Behavioural Processes.

[17]  Bruce L. McNaughton,et al.  Corrigendum: neuronal Mechanisms Underlying the Interaction between Visual Landmarks and Path Integration in the rat , 1996, Int. J. Neural Syst..

[18]  R. Muller,et al.  Place cell discharge is extremely variable during individual passes of the rat through the firing field. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  P. Somogyi,et al.  Defined types of cortical interneurone structure space and spike timing in the hippocampus , 2005, The Journal of physiology.

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

[21]  Emery N. Brown,et al.  Estimating a State-space Model from Point Process Observations Emery N. Brown , 2022 .

[22]  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.

[23]  E. Moser,et al.  A manifold of spatial maps in the brain , 2010, Trends in Cognitive Sciences.

[24]  J. Csicsvari,et al.  Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus , 2008, Nature Neuroscience.

[25]  Manuel Graña,et al.  Variable speed wind turbine controller adaptation by reinforcement learning , 2016, Integr. Comput. Aided Eng..

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

[27]  Anoopum S. Gupta,et al.  Segmentation of spatial experience by hippocampal theta sequences , 2012, Nature Neuroscience.

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

[29]  Dorian Kodelja,et al.  Multiagent cooperation and competition with deep reinforcement learning , 2015, PloS one.

[30]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 2005, IEEE Transactions on Neural Networks.

[31]  Anthony N. Burkitt,et al.  Delay analysis in the auditory brainstem of the rat: comparison with click latency , 2001, Hearing Research.

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

[33]  Wen-Hung Chao,et al.  Automatic spike sorting for extracellular electrophysiological recording using unsupervised single linkage clustering based on grey relational analysis , 2011, Journal of neural engineering.

[34]  G. Buzsáki,et al.  Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. , 2004, Journal of neurophysiology.

[35]  E.N. Brown,et al.  An analysis of hippocampal spatio-temporal representations using a Bayesian algorithm for neural spike train decoding , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[36]  J. B. Ranck,et al.  Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats , 1975, Experimental Neurology.

[37]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

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

[39]  Elijah A. Petter,et al.  Integrating Models of Interval Timing and Reinforcement Learning , 2018, Trends in Cognitive Sciences.

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

[41]  Minija Tamosiunaite,et al.  Odor supported place cell model and goal navigation in rodents , 2008, Journal of Computational Neuroscience.

[42]  Patrick Latuske,et al.  Interspike Intervals Reveal Functionally Distinct Cell Populations in the Medial Entorhinal Cortex , 2015, The Journal of Neuroscience.

[43]  C. Barry,et al.  Theta phase precession of grid and place cell firing in open environments , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Michael E. Hasselmo,et al.  Decoding Movement Trajectories Through a T-Maze Using Point Process Filters Applied to Place Field Data from Rat Hippocampal Region CA1 , 2009, Neural Computation.

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

[46]  C. McBain,et al.  Navigating the circuitry of the brain's GPS system: Future challenges for neurophysiologists , 2015, Hippocampus.

[47]  Ali Yousefi,et al.  Efficient Decoding of Multi-Dimensional Signals From Population Spiking Activity Using a Gaussian Mixture Particle Filter , 2019, IEEE Transactions on Biomedical Engineering.

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

[49]  Lo J. Bour,et al.  Automatic noise-level detection for extra-cellular micro-electrode recordings , 2009, Medical and Biological Engineering and Computing.

[50]  Lin Tian,et al.  Functional imaging of hippocampal place cells at cellular resolution during virtual navigation , 2010, Nature Neuroscience.

[51]  J. Lisman,et al.  Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. , 2000, Journal of neurophysiology.

[52]  A. Redish,et al.  Manipulating Decisiveness in Decision Making: Effects of Clonidine on Hippocampal Search Strategies , 2016, The Journal of Neuroscience.

[53]  Manuel Graña,et al.  Experiments of conditioned reinforcement learning in continuous space control tasks , 2018, Neurocomputing.

[54]  H. T. Blair,et al.  Conversion of a phase‐ to a rate‐coded position signal by a three‐stage model of theta cells, grid cells, and place cells , 2008, Hippocampus.

[55]  H Eichenbaum,et al.  The organization of spatial coding in the hippocampus: a study of neural ensemble activity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  A. Czurkó,et al.  Complementary spatial firing in place cell–interneuron pairs , 2010, The Journal of physiology.

[57]  Nachum Ulanovsky,et al.  Encoding of Head Direction by Hippocampal Place Cells in Bats , 2014, The Journal of Neuroscience.

[58]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[59]  Michael E Hasselmo,et al.  Computation by oscillations: Implications of experimental data for theoretical models of grid cells , 2008, Hippocampus.

[60]  Antal Berényi,et al.  Spatial coding and physiological properties of hippocampal neurons in the Cornu Ammonis subregions , 2016, Hippocampus.

[61]  M. Wilson,et al.  Spatial selectivity and theta phase precession in CA1 interneurons , 2007, Hippocampus.

[62]  Neil Burgess,et al.  Modelling spatial navigation by the rat hippocampus , 1995 .

[63]  Maria V. Sanchez-Vives,et al.  Source (or Part of the following Source): Type Article Title Real-time Position Reconstruction with Hippocampal Place Cells. Author(s) Real-time Position Reconstruction with Hippocampal Place Cells , 2022 .

[64]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

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

[66]  Neil Burgess,et al.  Using Grid Cells for Navigation , 2015, Neuron.

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

[68]  Bryan C. Souza,et al.  Asymmetry of the temporal code for space by hippocampal place cells , 2016, Scientific Reports.

[69]  J. O’Keefe,et al.  Space in the brain: how the hippocampal formation supports spatial cognition , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[70]  Louise Poissant Part I , 1996, Leonardo.

[71]  Albert K. Lee,et al.  Whole-Cell Recordings in Freely Moving Rats , 2006, Neuron.

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

[73]  P.E. Jercog,et al.  Heading direction with respect to a reference point modulates place-cell activity , 2018 .

[74]  Paul F. M. J. Verschure,et al.  A Model of Grid Cells Based on a Twisted Torus Topology , 2007, Int. J. Neural Syst..

[75]  Peter Vamplew,et al.  Concurrent Q‐learning: Reinforcement learning for dynamic goals and environments , 2005, Int. J. Intell. Syst..

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

[77]  Peter Dayan,et al.  Q-learning , 1992, Machine Learning.

[78]  Andrew P Maurer,et al.  Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells , 2006, The Journal of Neuroscience.

[79]  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.