Spike Train SIMilarity Space (SSIMS): A Framework for Single Neuron and Ensemble Data Analysis

Increased emphasis on circuit level activity in the brain makes it necessary to have methods to visualize and evaluate large-scale ensemble activity beyond that revealed by raster-histograms or pairwise correlations. We present a method to evaluate the relative similarity of neural spiking patterns by combining spike train distance metrics with dimensionality reduction. Spike train distance metrics provide an estimate of similarity between activity patterns at multiple temporal resolutions. Vectors of pair-wise distances are used to represent the intrinsic relationships between multiple activity patterns at the level of single units or neuronal ensembles. Dimensionality reduction is then used to project the data into concise representations suitable for clustering analysis as well as exploratory visualization. Algorithm performance and robustness are evaluated using multielectrode ensemble activity data recorded in behaving primates. We demonstrate how spike train SIMilarity space (SSIMS) analysis captures the relationship between goal directions for an eight-directional reaching task and successfully segregates grasp types in a 3D grasping task in the absence of kinematic information. The algorithm enables exploration of virtually any type of neural spiking (time series) data, providing similarity-based clustering of neural activity states with minimal assumptions about potential information encoding models.

[1]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[2]  Byron M. Yu,et al.  Techniques for extracting single-trial activity patterns from large-scale neural recordings , 2007, Current Opinion in Neurobiology.

[3]  Michael J. Black,et al.  Decoding Complete Reach and Grasp Actions from Local Primary Motor Cortex Populations , 2010, The Journal of Neuroscience.

[4]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[5]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[6]  Daniel W Moran,et al.  Strategy-Dependent Encoding of Planned Arm Movements in the Dorsal Premotor Cortex , 2012, Science.

[7]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[8]  Matthew T. Kaufman,et al.  Cortical Preparatory Activity: Representation of Movement or First Cog in a Dynamical Machine? , 2010, Neuron.

[9]  J. Donoghue,et al.  Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions , 2004, Experimental Brain Research.

[10]  Hansjörg Scherberger,et al.  Context-Specific Grasp Movement Representation in Macaque Ventral Premotor Cortex , 2010, The Journal of Neuroscience.

[11]  Juliana Dushanova,et al.  Neurons in primary motor cortex engaged during action observation , 2010, The European journal of neuroscience.

[12]  John P. Donoghue,et al.  Automated spike sorting using density grid contour clustering and subtractive waveform decomposition , 2007, Journal of Neuroscience Methods.

[13]  J. DiCarlo,et al.  Unsupervised Natural Visual Experience Rapidly Reshapes Size-Invariant Object Representation in Inferior Temporal Cortex , 2010, Neuron.

[14]  Philipp J. Keller,et al.  Whole-brain functional imaging at cellular resolution using light-sheet microscopy , 2013, Nature Methods.

[15]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[16]  I. Biederman,et al.  Representation of regular and irregular shapes in macaque inferotemporal cortex. , 2005, Cerebral cortex.

[17]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[18]  Jonathan D Victor,et al.  Spike train metrics , 2005, Current Opinion in Neurobiology.

[19]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

[20]  Wei Wu,et al.  Bayesian Population Decoding of Motor Cortical Activity Using a Kalman Filter , 2006, Neural Computation.

[21]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[22]  B. Weber,et al.  Context-dependent force coding in motor and premotor cortical areas , 1999, Experimental Brain Research.

[23]  S. R. Lehky,et al.  Comparison of shape encoding in primate dorsal and ventral visual pathways. , 2007, Journal of neurophysiology.

[24]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[25]  Sidney R. Lehky,et al.  Population Coding and the Labeling Problem: Extrinsic Versus Intrinsic Representations , 2013, Neural Computation.

[26]  Drew N. Robson,et al.  Brain-wide neuronal dynamics during motor adaptation in zebrafish , 2012, Nature.

[27]  Benjamin F. Grewe,et al.  High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision , 2010, Nature Methods.

[28]  Paul S. Weiss,et al.  The Brain Activity Map , 2013, Science.

[29]  Brain activity. , 2014, Nature nanotechnology.

[30]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[31]  J P Donoghue,et al.  Immediate and delayed changes of rat motor cortical output representation with new forelimb configurations. , 1992, Cerebral cortex.

[32]  Jonathan D. Victor,et al.  Metric-space analysis of spike trains: theory, algorithms and application , 1998, q-bio/0309031.

[33]  John P Donoghue,et al.  Cue to action processing in motor cortex populations. , 2014, Journal of neurophysiology.

[34]  R. Vogels,et al.  Inferotemporal neurons represent low-dimensional configurations of parameterized shapes , 2001, Nature Neuroscience.

[35]  M. Young,et al.  Sparse population coding of faces in the inferotemporal cortex. , 1992, Science.

[36]  S. Nelson,et al.  Dynamics of neuronal processing in rat somatosensory cortex , 1999, Trends in Neurosciences.

[37]  Tejas Khot,et al.  Visualizing high-dimensional data , 2016, XRDS.

[38]  Jun Tanji,et al.  Involvement of the Globus Pallidus in Behavioral Goal Determination and Action Specification , 2013, The Journal of Neuroscience.

[39]  J. Donoghue,et al.  Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates , 2013, Journal of neural engineering.

[40]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[42]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[43]  Stephen H. Scott,et al.  Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching , 1999, Journal of Neuroscience Methods.

[44]  Georgios A Keliris,et al.  Neurons in macaque area V4 acquire directional tuning after adaptation to motion stimuli , 2005, Nature Neuroscience.

[45]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.