Ensemble Spiking Research Articles

Adaptive modeling and inference of higher-order coordination in neuronal assemblies: A dynamic greedy estimation approach.

Central in the study of population codes, coordinated ensemble spiking activity is widely observable in neural recordings with hypothesized roles in robust stimulus representation, interareal communication, and learning and memory formation. Model-free measures of synchrony characterize coherent pairwise activity but not higher-order interactions, a limitation transcended by statistical models of ensemble spiking activity. However, existing model-based analyses often impose assumptions about the relevance of higher-order interactions and require repeated trials to characterize dynamics in the correlational structure of ensemble activity. To address these shortcomings, we propose an adaptive greedy filtering algorithm based on a discretized mark point-process model of ensemble spiking and a corresponding statistical inference framework to identify significant higher-order coordination. In the course of developing a precise statistical test, we show that confidence intervals can be constructed for greedily estimated parameters. We demonstrate the utility of our proposed methods on simulated neuronal assemblies. Applied to multi-electrode recordings from human and rat cortical assemblies, our proposed methods provide new insights into the dynamics underlying localized population activity during transitions between brain states.

FPGA-based fast bin-ratio spiking ensemble network for radioisotope identification

In this work, we demonstrate the training, conversion, and implementation flow of an FPGA-based bin-ratio ensemble spiking neural network applied for radioisotope identification. The combination of techniques including learned step quantisation (LSQ) and pruning facilitated the implementation by compressing the network’s parameters down to 30% yet retaining the accuracy of 97.04% with an accuracy loss of less than 1%. Meanwhile, the proposed ensemble network of 20 3-layer spiking neural networks (SNNs), which incorporates 1160 spiking neurons, only needs 334 μs for a single inference with the given clock frequency of 100 MHz. Under such optimisation, this FPGA implementation in an Artix-7 board consumes 157 μJ per inference by estimation.

Hippocampal and medial prefrontal ensemble spiking represents episodes and rules in similar task spaces

Episodic memory requires the hippocampus and prefrontal cortex to guide decisions by representing events in spatial, temporal, and personal contexts. Both brain regions have been described by cognitive theories that represent events in context as locations in maps or memory spaces. We query whether ensemble spiking in these regions described spatial structures as rats performed memory tasks. From each ensemble, we construct a state-space with each point defined by the coordinated spiking of single and pairs of units in 125-ms bins and investigate how state-space locations discriminate task features. Trajectories through state-spaces correspond with behavioral episodes framed by spatial, temporal, and internal contexts. Both hippocampal and prefrontal ensembles distinguish maze locations, task intervals, and goals by distances between state-space locations, consistent with cognitive mapping and relational memory space theories of episodic memory. Prefrontal modulation of hippocampal activity may guide choices by directing memory representations toward appropriate state-space goal locations.

Temporal progression along discrete coding states during decision-making in the mouse gustatory cortex.

The mouse gustatory cortex (GC) is involved in taste-guided decision-making in addition to sensory processing. Rodent GC exhibits metastable neural dynamics during ongoing and stimulus-evoked activity, but how these dynamics evolve in the context of a taste-based decision-making task remains unclear. Here we employ analytical and modeling approaches to i) extract metastable dynamics in ensemble spiking activity recorded from the GC of mice performing a perceptual decision-making task; ii) investigate the computational mechanisms underlying GC metastability in this task; and iii) establish a relationship between GC dynamics and behavioral performance. Our results show that activity in GC during perceptual decision-making is metastable and that this metastability may serve as a substrate for sequentially encoding sensory, abstract cue, and decision information over time. Perturbations of the model's metastable dynamics indicate that boosting inhibition in different coding epochs differentially impacts network performance, explaining a counterintuitive effect of GC optogenetic silencing on mouse behavior.

Disrupted social memory ensembles in the ventral hippocampus underlie social amnesia in autism-associated Shank3 mutant mice

The ability to remember conspecifics is critical for adaptive cognitive functioning and social communication, and impairments of this ability are hallmarks of autism spectrum disorders (ASDs). Although hippocampal ventral CA1 (vCA1) neurons are known to store social memories, how their activities are coordinated remains unclear. Here we show that vCA1 social memory neurons, characterized by enhanced activity in response to memorized individuals, were preferentially reactivated during sharp-wave ripples (SPW-Rs). Spike sequences of these social replays reflected the temporal orders of neuronal activities within theta cycles during social experiences. In ASD model Shank3 knockout mice, the proportion of social memory neurons was reduced, and neuronal ensemble spike sequences during SPW-Rs were disrupted, which correlated with impaired discriminatory social behavior. These results suggest that SPW-R-mediated sequential reactivation of neuronal ensembles is a canonical mechanism for coordinating hippocampus-dependent social memories and its disruption underlie the pathophysiology of social memory defects associated with ASD.

Coordinated increase of reliable cortical and striatal ensemble activations during recovery after stroke.

SUMMARYSkilled movements rely on a coordinated cortical and subcortical network, but how this network supports motor recovery after stroke is unknown. Previous studies focused on the perilesional cortex (PLC), but precisely how connected subcortical areas reorganize and coordinate with PLC is unclear. The dorsolateral striatum (DLS) is of interest because it receives monosynaptic inputs from motor cortex and is important for learning and generation of fast reliable actions. Using a rat focal stroke model, we perform chronic electrophysiological recordings in motor PLC and DLS during long-term recovery of a dexterous skill. We find that recovery is associated with the simultaneous emergence of reliable movement-related single-trial ensemble spiking in both structures along with increased cross-area alignment of spiking. Our study highlights the importance of consistent neural activity patterns across brain structures during recovery and suggests that modulation of cross-area coordination can be a therapeutic target for enhancing motor function post-stroke.

Dynamics of motor cortical activity during naturalistic feeding behavior

Objective. The orofacial primary motor cortex (MIo) plays a critical role in controlling tongue and jaw movements during oral motor functions, such as chewing, swallowing and speech. However, the neural mechanisms of MIo during naturalistic feeding are still poorly understood. There is a strong need for a systematic study of motor cortical dynamics during feeding behavior. Approach. To investigate the neural dynamics and variability of MIo neuronal activity during naturalistic feeding, we used chronically implanted micro-electrode arrays to simultaneously recorded ensembles of neuronal activity in the MIo of two monkeys (Macaca mulatta) while eating various types of food. We developed a Bayesian nonparametric latent variable model to reveal latent structures of neuronal population activity of the MIo and identify the complex mapping between MIo ensemble spike activity and high-dimensional kinematics. Main results. Rhythmic neuronal firing patterns and oscillatory dynamics are evident in single-unit activity. At the population level, we uncovered the neural dynamics of rhythmic chewing, and quantified the neural variability at multiple timescales (complete feeding sequences, chewing sequence stages, chewing gape cycle phases) across food types. Our approach accommodates time-warping of chewing sequences and automatic model selection, and maps the latent states to chewing behaviors at fine timescales. Significance. Our work shows that neural representations of MIo ensembles display spatiotemporal patterns in chewing gape cycles at different chew sequence stages, and these patterns vary in a stage-dependent manner. Unsupervised learning and decoding analysis may reveal the link between complex MIo spatiotemporal patterns and chewing kinematics.

Real-Time Readout of Large-Scale Unsorted Neural Ensemble Place Codes

Uncovering spatial representations from large-scale ensemble spike activity in specific brain circuits provides valuable feedback in closed-loop experiments. We develop a graphics processing unit (GPU)-powered population-decoding system for ultrafast reconstruction of spatial positions from rodents' unsorted spatiotemporal spiking patterns, during run behavior or sleep. In comparison with an optimized quad-core central processing unit (CPU) implementation, our approach achieves an ∼20- to 50-fold increase in speed in eight tested rat hippocampal, cortical, and thalamic ensemble recordings, with real-time decoding speed (approximately fraction of a millisecond per spike) and scalability up to thousands of channels. Byaccommodating parallel shuffling in real time (computation time <15ms), our approach enables assessment of the statistical significance of online-decoded "memory replay" candidates during quiet wakefulness or sleep. This open-source software toolkit supports the decoding of spatial correlates or content-triggered experimental manipulation in closed-loop neuroscience experiments.

Real-time classification of experience-related ensemble spiking patterns for closed-loop applications.

Communication in neural circuits across the cortex is thought to be mediated by spontaneous temporally organized patterns of population activity lasting ~50 -200 ms. Closed-loop manipulations have the unique power to reveal direct and causal links between such patterns and their contribution to cognition. Current brain-computer interfaces, however, are not designed to interpret multi-neuronal spiking patterns at the millisecond timescale. To bridge this gap, we developed a system for classifying ensemble patterns in a closed-loop setting and demonstrated its application in the online identification of hippocampal neuronal replay sequences in the rat. Our system decodes multi-neuronal patterns at 10 ms resolution, identifies within 50 ms experience-related patterns with over 70% sensitivity and specificity, and classifies their content with 95% accuracy. This technology scales to high-count electrode arrays and will help to shed new light on the contribution of internally generated neural activity to coordinated neural assembly interactions and cognition.

Conjunctive coding in an evolved spiking model of retrosplenial cortex.

Retrosplenial cortex (RSC) is an association cortex supporting spatial navigation and memory. However, critical issues remain concerning the forms by which its ensemble spiking patterns register spatial relationships that are difficult for experimental techniques to fully address. We therefore applied an evolutionary algorithmic optimization technique to create spiking neural network models that matched electrophysiologically observed spiking dynamics in rat RSC neuronal ensembles. Virtual experiments conducted on the evolved networks revealed a mixed selectivity coding capability that was not built into the optimization method, but instead emerged as a consequence of replicating biological firing patterns. The experiments reveal several important outcomes of mixed selectivity that may subserve flexible navigation and spatial representation: (a) robustness to loss of specific inputs, (b) immediate and stable encoding of novel routes and route locations, (c) automatic resolution of input variable conflicts, and (d) dynamic coding that allows rapid adaptation to changing task demands without retraining. These findings suggest that biological retrosplenial cortex can generate unique, first-trial, conjunctive encodings of spatial positions and actions that can be used by downstream brain regions for navigation and path integration. Moreover, these results are consistent with the proposed role for the RSC in the transformation of representations between reference frames and navigation strategy deployment. Finally, the specific modeling framework used for evolving synthetic retrosplenial networks represents an important advance for computational modeling by which synthetic neural networks can encapsulate, describe, and predict the behavior of neural circuits at multiple levels of function. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Unsupervised clustering of temporal patterns in high-dimensional neuronal ensembles using a novel dissimilarity measure.

Temporally ordered multi-neuron patterns likely encode information in the brain. We introduce an unsupervised method, SPOTDisClust (Spike Pattern Optimal Transport Dissimilarity Clustering), for their detection from high-dimensional neural ensembles. SPOTDisClust measures similarity between two ensemble spike patterns by determining the minimum transport cost of transforming their corresponding normalized cross-correlation matrices into each other (SPOTDis). Then, it performs density-based clustering based on the resulting inter-pattern dissimilarity matrix. SPOTDisClust does not require binning and can detect complex patterns (beyond sequential activation) even when high levels of out-of-pattern “noise” spiking are present. Our method handles efficiently the additional information from increasingly large neuronal ensembles and can detect a number of patterns that far exceeds the number of recorded neurons. In an application to neural ensemble data from macaque monkey V1 cortex, SPOTDisClust can identify different moving stimulus directions on the sole basis of temporal spiking patterns.

Rate and Temporal Coding Mechanisms in the Anterior Cingulate Cortex for Pain Anticipation

Pain is a complex sensory and affective experience. Through its anticipation, animals can learn to avoid pain. Much is known about passive avoidance during a painful event; however, less is known about active pain avoidance. The anterior cingulate cortex (ACC) is a critical hub for affective pain processing. However, there is currently no mechanism that links ACC activities at the cellular level with behavioral anticipation or avoidance. Here we asked whether distinct populations of neurons in the ACC can encode information for pain anticipation. We used tetrodes to record from ACC neurons during a conditioning assay to train rats to avoid pain. We found that in rats that successfully avoid acute pain episodes, neurons that responded to pain shifted their firing rates to an earlier time, whereas neurons that responded to the anticipation of pain increased their firing rates prior to noxious stimulation. Furthermore, we found a selected group of neurons that shifted their firing from a pain-tuned response to an anticipatory response. Unsupervised learning analysis of ensemble spike activity indicates that temporal spiking patterns of ACC neurons can indeed predict the onset of pain avoidance. These results suggest rate and temporal coding schemes in the ACC for pain avoidance.

Real-time particle filtering and smoothing algorithms for detecting abrupt changes in neural ensemble spike activity.

Sequential change-point detection from time series data is a common problem in many neuroscience applications, such as seizure detection, anomaly detection, and pain detection. In our previous work (Chen Z, Zhang Q, Tong AP, Manders TR, Wang J. J Neural Eng 14: 036023, 2017), we developed a latent state-space model, known as the Poisson linear dynamical system, for detecting abrupt changes in neuronal ensemble spike activity. In online brain-machine interface (BMI) applications, a recursive filtering algorithm is used to track the changes in the latent variable. However, previous methods have been restricted to Gaussian dynamical noise and have used Gaussian approximation for the Poisson likelihood. To improve the detection speed, we introduce non-Gaussian dynamical noise for modeling a stochastic jump process in the latent state space. To efficiently estimate the state posterior that accommodates non-Gaussian noise and non-Gaussian likelihood, we propose particle filtering and smoothing algorithms for the change-point detection problem. To speed up the computation, we implement the proposed particle filtering algorithms using advanced graphics processing unit computing technology. We validate our algorithms, using both computer simulations and experimental data for acute pain detection. Finally, we discuss several important practical issues in the context of real-time closed-loop BMI applications. NEW & NOTEWORTHY Sequential change-point detection is an important problem in closed-loop neuroscience experiments. This study proposes novel sequential Monte Carlo methods to quickly detect the onset and offset of a stochastic jump process that drives the population spike activity. This new approach is robust with respect to spike sorting noise and varying levels of signal-to-noise ratio. The GPU implementation of the computational algorithm allows for parallel processing in real time.

Deciphering neuronal population codes for acute thermal pain

Objective. Pain is defined as an unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage. Current pain research mostly focuses on molecular and synaptic changes at the spinal and peripheral levels. However, a complete understanding of pain mechanisms requires the physiological study of the neocortex. Our goal is to apply a neural decoding approach to read out the onset of acute thermal pain signals, which can be used for brain–machine interface. Approach. We used micro wire arrays to record ensemble neuronal activities from the primary somatosensory cortex (S1) and anterior cingulate cortex (ACC) in freely behaving rats. We further investigated neural codes for acute thermal pain at both single-cell and population levels. To detect the onset of acute thermal pain signals, we developed a novel latent state-space framework to decipher the sorted or unsorted S1 and ACC ensemble spike activities, which reveal information about the onset of pain signals. Main results. The state space analysis allows us to uncover a latent state process that drives the observed ensemble spike activity, and to further detect the ‘neuronal threshold’ for acute thermal pain on a single-trial basis. Our method achieved good detection performance in sensitivity and specificity. In addition, our results suggested that an optimal strategy for detecting the onset of acute thermal pain signals may be based on combined evidence from S1 and ACC population codes. Significance. Our study is the first to detect the onset of acute pain signals based on neuronal ensemble spike activity. It is important from a mechanistic viewpoint as it relates to the significance of S1 and ACC activities in the regulation of the acute pain onset.

Robust Estimation of Sparse Narrowband Spectra from Neuronal Spiking Data.

Characterizing the spectral properties of neuronal responses is an important problem in computational neuroscience, as it provides insight into the spectral organization of the underlying functional neural processes. Although spectral analysis techniques are widely used in the analysis of noninvasive neural recordings such as EEG, their application to spiking data is limited due to the binary and nonlinear nature of neuronal spiking. In this paper, we address the problem of estimating the power spectral density of the neural covariate driving the spiking statistics of a neuronal population from binary observations. We consider a neuronal ensemble spiking according to Bernoulli statistics, for which the conditional intensity function is given by the logistic map of a harmonic second-order stationary process with sparse narrowband spectra. By employing sparsity-promoting priors, we compute the maximum a posteriori estimate of the power spectral density of the process from the binary spiking observations. Furthermore, we construct confidence intervals for these estimates by an efficient posterior sampling procedure. We provide simulation studies which reveal that our method outperforms the existing methods for extracting the frequency content of spiking data. Application of our method to clinically recorded spiking data from a patient under general anesthesia reveals a striking resemblance between our estimated power spectral density and that of the local field potential signal. This result corroborates existing findings regarding the salient role of the local field potential as a major neural covariate of rhythmic cortical spiking activity under anesthesia. Our technique allows us to analyze the harmonic structure of spiking activity in a robust fashion, independently of the local field potentials, and without any prior assumption of the spectral spread and content of the underlying neural processes. Other than its usage in the spectral analysis of neuronal spiking data, our technique can be applied to a wide variety of binary data, such as heart beat data, in order to obtain a robust spectral representation.

Uncovering representations of sleep-associated hippocampal ensemble spike activity.

Pyramidal neurons in the rodent hippocampus exhibit spatial tuning during spatial navigation, and they are reactivated in specific temporal order during sharp-wave ripples observed in quiet wakefulness or slow wave sleep. However, analyzing representations of sleep-associated hippocampal ensemble spike activity remains a great challenge. In contrast to wake, during sleep there is a complete absence of animal behavior, and the ensemble spike activity is sparse (low occurrence) and fragmental in time. To examine important issues encountered in sleep data analysis, we constructed synthetic sleep-like hippocampal spike data (short epochs, sparse and sporadic firing, compressed timescale) for detailed investigations. Based upon two Bayesian population-decoding methods (one receptive field-based, and the other not), we systematically investigated their representation power and detection reliability. Notably, the receptive-field-free decoding method was found to be well-tuned for hippocampal ensemble spike data in slow wave sleep (SWS), even in the absence of prior behavioral measure or ground truth. Our results showed that in addition to the sample length, bin size, and firing rate, number of active hippocampal pyramidal neurons are critical for reliable representation of the space as well as for detection of spatiotemporal reactivated patterns in SWS or quiet wakefulness.

Low- and high-gamma oscillations deviate in opposite directions from zero-phase synchrony in the limbic corticostriatal loop.

The loop structure of cortico-striatal anatomy in principle enables both descending (cortico-striatal) and ascending (striato-cortical) influences, but the factors that regulate the flow of information in these loops are not known. We report that low- and high-gamma oscillations (∼50 and ∼80 Hz, respectively) in the local field potential of freely moving rats are highly synchronous between the infralimbic region of the medial prefrontal cortex (mPFC) and the ventral striatum (vStr). Strikingly, high-gamma oscillations in mPFC preceded those in vStr, whereas low-gamma oscillations in mPFC lagged those in vStr, with short (∼1 ms) time lags. These systematic deviations from zero-phase synchrony were consistent across measures based on amplitude cross-correlation and phase slopes and were robustly maintained between behavioral states and different individual subjects. Furthermore, low- and high-gamma oscillations were associated with distinct ensemble spiking patterns in vStr, even when controlling for overt behavioral differences and slow changes in neural activity. These results imply that neural activity in vStr and mPFC is tightly coupled at the gamma timescale and raise the intriguing possibility that frequency-specific deviations from this coupling may signal transient leader-follower switches.

A Bayesian nonparametric approach for uncovering rat hippocampal population codes during spatial navigation

BackgroundRodent hippocampal population codes represent important spatial information about the environment during navigation. Computational methods have been developed to uncover the neural representation of spatial topology embedded in rodent hippocampal ensemble spike activity. New methodWe extend our previous work and propose a novel Bayesian nonparametric approach to infer rat hippocampal population codes during spatial navigation. To tackle the model selection problem, we leverage a Bayesian nonparametric model. Specifically, we apply a hierarchical Dirichlet process-hidden Markov model (HDP-HMM) using two Bayesian inference methods, one based on Markov chain Monte Carlo (MCMC) and the other based on variational Bayes (VB). ResultsThe effectiveness of our Bayesian approaches is demonstrated on recordings from a freely behaving rat navigating in an open field environment. Comparison with existing methodsThe HDP-HMM outperforms the finite-state HMM in both simulated and experimental data. For HPD-HMM, the MCMC-based inference with Hamiltonian Monte Carlo (HMC) hyperparameter sampling is flexible and efficient, and outperforms VB and MCMC approaches with hyperparameters set by empirical Bayes. ConclusionThe Bayesian nonparametric HDP-HMM method can efficiently perform model selection and identify model parameters, which can used for modeling latent-state neuronal population dynamics.

An FPGA-Based High-Performance Neural Ensemble Spiking Activity Simulator Utilizing Generalized Volterra Kernel and Complexity Analysis

Neural information is represented and transmitted among neuronal units by a series of all-or-none “neural codes”. During the process of neural prosthesis design, generally, a large amount of “neural codes” need to be captured and analyzed, which brings about an important discipline, known as neuroinformatics. However, in neuroinformatics study, this coding process, also termed as “spiking activity”, is not straightforward for prediction. It is owing to the high nonlinearity and dynamic property involved in generation of the neuronal spikes. In this paper, a novel generalized Volterra kernel-based neural spiking activity simulator is introduced for prediction of the neural codes in mammalian hippocampal region. High-performance VLSI architecture is established for the simulator based on high-order Volterra kernels involving cross-terms. The effectiveness and efficiency of the simulator are proven in experimental settings. This simulator has the potential to serve as a core functional unit in future hippocampal cognitive neural prosthesis.

Kernel density compression for real-time Bayesian encoding/decoding of unsorted hippocampal spikes

To gain a better understanding of how neural ensembles communicate and process information, neural decoding algorithms are used to extract information encoded in their spiking activity. Bayesian decoding is one of the most used neural population decoding approaches to extract information from the ensemble spiking activity of rat hippocampal neurons. Recently it has been shown how Bayesian decoding can be implemented without the intermediate step of sorting spike waveforms into groups of single units. Here we extend the approach in order to make it suitable for online encoding/decoding scenarios that require real-time decoding such as brain-machine interfaces. We propose an online algorithm for the Bayesian decoding that reduces the time required for decoding neural populations, resulting in a real-time capable decoding framework. More specifically, we improve the speed of the probability density estimation step, which is the most essential and the most expensive computation of the spike-sorting-less decoding process, by developing a kernel density compression algorithm. In contrary to existing online kernel compression techniques, rather than optimizing for the minimum estimation error caused by kernels compression, the proposed method compresses kernels on the basis of the distance between the merging component and its most similar neighbor. Thus, without costly optimization, the proposed method has very low compression latency with a small and manageable estimation error. In addition, the proposed bandwidth matching method for Gaussian kernels merging has an interesting mathematical property whereby optimization in the estimation of the probability density function can be performed efficiently, resulting in a faster decoding speed. We successfully applied the proposed kernel compression algorithm to the Bayesian decoding framework to reconstruct positions of a freely moving rat from hippocampal unsorted spikes, with significant improvements in the decoding speed and acceptable decoding error.