Rapid classification of hippocampal replay content for real-time applications.

Sharp-wave ripple (SWR) events in the hippocampus replay millisecond-timescale patterns of place cell activity related to the past experience of an animal. Interrupting SWR events leads to learning and memory impairments, but how the specific patterns of place cell spiking seen during SWRs contribute to learning and memory remains unclear. A deeper understanding of this issue will require the ability to manipulate SWR events based on their content. Accurate real-time decoding of SWR replay events requires new algorithms that are able to estimate replay content and the associated uncertainty, along with software and hardware that can execute these algorithms for biological interventions on a millisecond timescale. Here we develop an efficient estimation algorithm to categorize the content of replay from multiunit spiking activity. Specifically, we apply real-time decoding methods to each SWR event and then compute the posterior probability of the replay feature. We illustrate this approach by classifying SWR events from data recorded in the hippocampus of a rat performing a spatial memory task into four categories: whether they represent outbound or inbound trajectories and whether the activity is replayed forward or backward in time. We show that our algorithm can classify the majority of SWR events in a recording epoch within 20 ms of the replay onset with high certainty, which makes the algorithm suitable for a real-time implementation with short latencies to incorporate into content-based feedback experiments.

[1]  L. Frank,et al.  Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus , 2009, Neuron.

[2]  L. Frank,et al.  New Experiences Enhance Coordinated Neural Activity in the Hippocampus , 2008, Neuron.

[3]  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.

[4]  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.

[5]  David J Foster,et al.  Hippocampal Replay Captures the Unique Topological Structure of a Novel Environment , 2014, The Journal of Neuroscience.

[6]  Emery N. Brown,et al.  Dynamic Analysis of Neural Encoding by Point Process Adaptive Filtering , 2004, Neural Computation.

[7]  Margaret F. Carr,et al.  Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval , 2011, Nature Neuroscience.

[8]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[9]  L. Paninski,et al.  Neural decoding of goal-directed movements using a linear state-space model with hidden states , 2007 .

[10]  Wei Wu,et al.  A new look at state-space models for neural data , 2010, Journal of Computational Neuroscience.

[11]  A. Redish.  Beyond the Cognitive Map: From Place Cells to Episodic Memory , 1999 .

[12]  R. Kass,et al.  Bayesian decoding of neural spike trains , 2010 .

[13]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[14]  M. Hasselmo.  A model of episodic memory: Mental time travel along encoded trajectories using grid cells , 2009, Neurobiology of Learning and Memory.

[15]  David S. Touretzky,et al.  The Role of the Hippocampus in Solving the Morris Water Maze , 1998, Neural Computation.

[16]  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.

[17]  G. Buzsáki.  Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

[18]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 2004, Experimental Brain Research.

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

[20]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[21]  Mattias P. Karlsson,et al.  Network Dynamics Underlying the Formation of Sparse, Informative Representations in the Hippocampus , 2008, The Journal of Neuroscience.

[22]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[23]  Daryl J. Daley,et al.  An Introduction to the Theory of Point Processes , 2013 .

[24]  Delia Silva,et al.  Trajectory events across hippocampal place-cells require previous experience , 2015, Nature Neuroscience.

[25]  Emery N. Brown,et al.  A State-Space Analysis for Reconstruction of Goal-Directed Movements Using Neural Signals , 2006, Neural Computation.

[26]  Wei Wu,et al.  Neural Decoding of Hand Motion Using a Linear State-Space Model With Hidden States , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[27]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[28]  Byron M. Yu,et al.  Detecting neural-state transitions using hidden Markov models for motor cortical prostheses. , 2008, Journal of neurophysiology.

[29]  S. Haykin,et al.  Adaptive Filter Theory , 1986 .

[30]  J. O’Neill,et al.  Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration , 2007, The European journal of neuroscience.

[31]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[32]  G. Buzsáki.  Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[33]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

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

[35]  Jean-René Martin,et al.  Drosophila CAKI/CMG protein, a homolog of human CASK, is essential for regulation of neurotransmitter vesicle release. , 2005, Journal of neurophysiology.

[36]  D. Billheimer.  Functional Data Analysis, 2nd edition edited by J. O. Ramsay and B. W. Silverman , 2007 .

[37]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[38]  G. Buzsáki.  Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[39]  Matthew A Wilson,et al.  Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus , 2014, eLife.

[40]  Karl Deisseroth,et al.  Closed-Loop and Activity-Guided Optogenetic Control , 2015, Neuron.

[41]  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.

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

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

[44]  Uri T. Eden,et al.  Clusterless Decoding of Position from Multiunit Activity Using a Marked Point Process Filter , 2015, Neural Computation.

[45]  J. Csicsvari,et al.  Massively parallel recording of unit and local field potentials with silicon-based electrodes. , 2003, Journal of neurophysiology.

[46]  B. Silverman,et al.  Functional Data Analysis , 1997 .

[47]  P. Best,et al.  Spatial processing in the brain: the activity of hippocampal place cells. , 2001, Annual review of neuroscience.

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

[49]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[50]  Mattias P. Karlsson,et al.  Awake replay of remote experiences in the hippocampus , 2009, Nature Neuroscience.

[51]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[52]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.