A Novel Nonparametric Approach for Neural Encoding and Decoding Models of Multimodal Receptive Fields

Pyramidal neurons recorded from the rat hippocampus and entorhinal cortex, such as place and grid cells, have diverse receptive fields, which are either unimodal or multimodal. Spiking activity from these cells encodes information about the spatial position of a freely foraging rat. At fine timescales, a neuron’s spike activity also depends significantly on its own spike history. However, due to limitations of current parametric modeling approaches, it remains a challenge to estimate complex, multimodal neuronal receptive fields while incorporating spike history dependence. Furthermore, efforts to decode the rat’s trajectory in one- or two-dimensional space from hippocampal ensemble spiking activity have mainly focused on spike history–independent neuronal encoding models. In this letter, we address these two important issues by extending a recently introduced nonparametric neural encoding framework that allows modeling both complex spatial receptive fields and spike history dependencies. Using this extended nonparametric approach, we develop novel algorithms for decoding a rat’s trajectory based on recordings of hippocampal place cells and entorhinal grid cells. Results show that both encoding and decoding models derived from our new method performed significantly better than state-of-the-art encoding and decoding models on 6 minutes of test data. In addition, our model’s performance remains invariant to the apparent modality of the neuron’s receptive field.

[1]  Matthias Bethge,et al.  Beyond GLMs: A Generative Mixture Modeling Approach to Neural System Identification , 2012, PLoS Comput. Biol..

[3]  Emery N. Brown,et al.  The effects of cues on neurons in the basal ganglia in Parkinson's disease , 2012, Front. Integr. Neurosci..

[4]  Rahul Agarwal,et al.  Mutual Dependence: A Novel Method for Computing Dependencies Between Random Variables , 2015, 1506.00673.

[5]  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.

[6]  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.

[7]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[8]  H. Akaike Block Toeplitz Matrix Inversion , 1973 .

[9]  J. Duhamel,et al.  Differential effects of parietal and frontal inactivations on reaction times distributions in a visual search task , 2012, Front. Integr. Neurosci..

[10]  Matthew A. Wilson,et al.  Dynamic Analyses of Information Encoding in Neural Ensembles , 2004, Neural Computation.

[11]  Robert E. Kass,et al.  A Spike-Train Probability Model , 2001, Neural Computation.

[12]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[13]  K. Kahn,et al.  Neuron selection for decoding dexterous finger movements , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[14]  R. Marks Introduction to Shannon Sampling and Interpolation Theory , 1990 .

[15]  C. D. Kemp,et al.  Density Estimation for Statistics and Data Analysis , 1987 .

[16]  M. Quirk,et al.  Construction and analysis of non-Poisson stimulus-response models of neural spiking activity , 2001, Journal of Neuroscience Methods.

[17]  Maneesh Sahani,et al.  Equating information-theoretic and likelihood-based methods for neural dimensionality reduction , 2013, 1308.3542.

[18]  Matthew A. Wilson,et al.  Transductive neural decoding for unsorted neuronal spikes of rat hippocampus , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[20]  Wulfram Gerstner,et al.  Rescaling, thinning or complementing? On goodness-of-fit procedures for point process models and Generalized Linear Models , 2010, NIPS.

[21]  Herbert F. Voigt,et al.  IEEE Engineering in Medicine and Biology Society , 2019, IEEE Transactions on Biomedical Engineering.

[22]  Sridevi V. Sarma,et al.  Restoring the basal ganglia in Parkinson's disease to normal via multi-input phase-shifted deep brain stimulation , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[23]  Todd P. Coleman,et al.  A Computationally Efficient Method for Nonparametric Modeling of Neural Spiking Activity with Point Processes , 2010, Neural Computation.

[24]  Sridevi V. Sarma,et al.  An analytical study of relay neuron's reliability: Dependence on input and model parameters , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[25]  David Vere-Jones,et al.  Point Processes , 2011, International Encyclopedia of Statistical Science.

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

[27]  Zhe Chen,et al.  Advanced state space methods for neural and clinical data , 2015 .

[28]  Do the spatial frequencies of grid cells mold the firing fields of place cells? , 2015, Proceedings of the National Academy of Sciences.

[29]  Emery N. Brown,et al.  The Time-Rescaling Theorem and Its Application to Neural Spike Train Data Analysis , 2002, Neural Computation.

[30]  William Bialek,et al.  Analyzing Neural Responses to Natural Signals: Maximally Informative Dimensions , 2002, Neural Computation.

[31]  B. McNaughton,et al.  Place field expansion after focal MEC inactivations is consistent with loss of Fourier components and path integrator gain reduction , 2015, Proceedings of the National Academy of Sciences.

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

[33]  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.

[34]  Erwin B. Montgomery,et al.  Non-stationary discharge patterns in motor cortex under subthalamic nucleus deep brain stimulation , 2012, Front. Integr. Neurosci..

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

[37]  Nitish V Thakor,et al.  PMv Neuronal Firing May Be Driven by a Movement Command Trajectory within Multidimensional Gaussian Fields , 2015, The Journal of Neuroscience.

[38]  Deniz Yuret,et al.  Dynamic Hill Climbing: Overcoming the limitations of optimization techniques , 1993 .

[39]  Sridevi V. Sarma,et al.  Performance Limitations of Relay Neurons , 2012, PLoS Comput. Biol..

[40]  Zhe Chen,et al.  An Overview of Bayesian Methods for Neural Spike Train Analysis , 2013, Comput. Intell. Neurosci..

[41]  Stephen P. Boyd,et al.  Convex Optimization , 2004, Algorithms and Theory of Computation Handbook.

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

[43]  Kamiar Rahnama Rad,et al.  Efficient, adaptive estimation of two-dimensional firing rate surfaces via Gaussian process methods , 2010, Network.

[44]  S. Sarma,et al.  Nonparametric Estimation of Band-limited Probability Density Functions , 2015, 1503.06236.

[45]  Sridevi V. Sarma,et al.  The effects of DBS patterns on basal ganglia activity and thalamic relay , 2011, Journal of Computational Neuroscience.

[46]  Ian H. Stevenson,et al.  Spatially Distributed Local Fields in the Hippocampus Encode Rat Position , 2014, Science.

[47]  P. McCullagh,et al.  Generalized Linear Models , 1984 .

[48]  Fabian Kloosterman,et al.  Bayesian decoding using unsorted spikes in the rat hippocampus. , 2014, Journal of neurophysiology.

[49]  Jonathan W. Pillow,et al.  Time-rescaling methods for the estimation and assessment of non-Poisson neural encoding models , 2009, NIPS.

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