Raster Plot Research Articles

Rastermap: a discovery method for neural population recordings.

Neurophysiology has long progressed through exploratory experiments and chance discoveries. Anecdotes abound of researchers listening to spikes in real time and noticing patterns of activity related to ongoing stimuli or behaviors. With the advent of large-scale recordings, such close observation of data has become difficult. To find patterns in large-scale neural data, we developed 'Rastermap', a visualization method that displays neurons as a raster plot after sorting them along a one-dimensional axis based on their activity patterns. We benchmarked Rastermap on realistic simulations and then used it to explore recordings of tens of thousands of neurons from mouse cortex during spontaneous, stimulus-evoked and task-evoked epochs. We also applied Rastermap to whole-brain zebrafish recordings; to wide-field imaging data; to electrophysiological recordings in rat hippocampus, monkey frontal cortex and various cortical and subcortical regions in mice; and to artificial neural networks. Finally, we illustrate high-dimensional scenarios where Rastermap and similar algorithms cannot be used effectively.

Nondifferentiable activity in the brain.

Spike raster plots of numerous neurons show vertical stripes, indicating that neurons exhibit synchronous activity in the brain. We seek to determine whether these coherent dynamics are caused by smooth brainwave activity or by something else. By analyzing biological data, we find that their cross-correlograms exhibit not only slow undulation but also a cusp at the origin, in addition to possible signs of monosynaptic connectivity. Here we show that undulation emerges if neurons are subject to smooth brainwave oscillations while a cusp results from nondifferentiable fluctuations. While modern analysis methods have achieved good connectivity estimation by adapting the models to slow undulation, they still make false inferences due to the cusp. We devise a new analysis method that may solve both problems. We also demonstrate that oscillations and nondifferentiable fluctuations may emerge in simulations of large-scale neural networks.

Open-Source Real-Time Closed-Loop Electrical Threshold Tracking for Translational Pain Research.

Nociceptors are a class of primary afferent neurons that signal potentially harmful noxious stimuli. An increase in nociceptor excitability occurs in acute and chronic pain conditions. This produces abnormal ongoing activity or reduced activation thresholds to noxious stimuli. Identifying the cause of this increased excitability is required for the development and validation of mechanism-based treatments. Single-neuron electrical threshold tracking can quantify nociceptor excitability. Therefore, we have developed an application to allow such measurements and demonstrate its use in humans and rodents. APTrack provides real-time data visualization and action potential identification using a temporal raster plot. Algorithms detect action potentials by threshold crossing and monitor their latency after electrical stimulation. The plugin then modulates the electrical stimulation amplitude using an up-down method to estimate the electrical threshold of the nociceptors. The software was built upon the Open Ephys system (V0.54) and coded in C++ using the JUCE framework. It runs on Windows, Linux, and Mac operating systems. The open-source code is available (https://github.com/Microneurography/APTrack). The electrophysiological recordings were taken from nociceptors in both a mouse skin-nerve preparation using the teased fiber method in the saphenous nerve and in healthy human volunteers using microneurography in the superficial peroneal nerve. Nociceptors were classified by their response to thermal and mechanical stimuli, as well as by monitoring the activity-dependent slowing of the conduction velocity. The software facilitated the experiment by simplifying the action potential identification through the temporal raster plot. We demonstrate real-time closed-loop electrical threshold tracking of single-neuron action potentials duringin vivohuman microneurography, for the first time, and duringex vivomouse electrophysiological recordings of C-fibers and Aδ-fibers. We establish proof of principle by showing that the electrical threshold of a human heat-sensitive C-fiber nociceptor is reduced by heating the receptive field. This plugin enables the electrical threshold tracking of single-neuron action potentials and allows the quantification of changes in nociceptor excitability.

Xenon LFP Analysis Platform Is a Novel Graphical User Interface for Analysis of Local Field Potential From Large-Scale MEA Recordings.

High-density multi-electrode array (HD-MEA) has enabled neuronal measurements at high spatial resolution to record local field potentials (LFP), extracellular action potentials, and network-wide extracellular recording on an extended spatial scale. While we have advanced recording systems with over 4,000 electrodes capable of recording data at over 20 kHz, it still presents computational challenges to handle, process, extract, and view information from these large recordings. We have created a computational method, and an open-source toolkit built in Python, rendered on a web browser using Plotly’s Dash for extracting and viewing the data and creating interactive visualization. In addition to extracting and viewing entire or small chunks of data sampled at lower or higher frequencies, respectively, it provides a framework to collect user inputs, analyze channel groups, generate raster plots, view quick summary measures for LFP activity, detect and isolate noise channels, and generate plots and visualization in both time and frequency domain. Incorporated into our Graphical User Interface (GUI), we also created a novel seizure detection method, which can be used to detect the onset of seizures in all or a selected group of channels and provide the following measures of seizures: distance, duration, and propagation across the region of interest. We demonstrate the utility of this toolkit, using datasets collected from an HD-MEA device comprising of 4,096 recording electrodes. For the current analysis, we demonstrate the toolkit and methods with a low sampling frequency dataset (300 Hz) and a group of approximately 400 channels. Using this toolkit, we present novel data demonstrating increased seizure propagation speed from brain slices of Scn1aHet mice compared to littermate controls. While there have been advances in HD-MEA recording systems with high spatial and temporal resolution, limited tools are available for researchers to view and process these big datasets. We now provide a user-friendly toolkit to analyze LFP activity obtained from large-scale MEA recordings with translatable applications to EEG recordings and demonstrate the utility of this new graphic user interface with novel biological findings.

Raster plots machine learning to predict the seizure liability of drugs and to identify drugs

In vitro microelectrode array (MEA) assessment using human induced pluripotent stem cell (iPSC)-derived neurons holds promise as a method of seizure and toxicity evaluation. However, there are still issues surrounding the analysis methods used to predict seizure and toxicity liability as well as drug mechanisms of action. In the present study, we developed an artificial intelligence (AI) capable of predicting the seizure liability of drugs and identifying drugs using deep learning based on raster plots of neural network activity. The seizure liability prediction AI had a prediction accuracy of 98.4% for the drugs used to train it, classifying them correctly based on their responses as either seizure-causing compounds or seizure-free compounds. The AI also made concentration-dependent judgments of the seizure liability of drugs that it was not trained on. In addition, the drug identification AI implemented using the leave-one-sample-out scheme could distinguish among 13 seizure-causing compounds as well as seizure-free compound responses, with a mean accuracy of 99.9 ± 0.1% for all drugs. These AI prediction models are able to identify seizure liability concentration-dependence, rank the level of seizure liability based on the seizure liability probability, and identify the mechanism of the action of compounds. This holds promise for the future of in vitro MEA assessment as a powerful, high-accuracy new seizure liability prediction method.

Seizure liability prediction method based on electrical activities in human iPS cell-derived neurons using machine learning -Comparison of raster plot model and parameter model-

seizure liability prediction method based on electrical activities in human iPS cell-derived neurons using machine learning -Comparison of raster plot model and parameter model-

Population and individual firing behaviors in sparsely synchronized rhythms in the hippocampal dentate gyrus.

We investigate population and individual firing behaviors in sparsely synchronized rhythms (SSRs) in a spiking neural network of the hippocampal dentate gyrus (DG). The main encoding granule cells (GCs) are grouped into lamellar clusters. In each GC cluster, there is one inhibitory (I) basket cell (BC) along with excitatory (E) GCs, and they form the E-I loop. Winner-take-all competition, leading to sparse activation of the GCs, occurs in each GC cluster. Such sparsity has been thought to enhance pattern separation performed in the DG. During the winner-take-all competition, SSRs are found to appear in each population of the GCs and the BCs through interaction of excitation of the GCs with inhibition of the BCs. Sparsely synchronized spiking stripes appear successively with the population frequency Hz) in the raster plots of spikes. We also note that excitatory hilar mossy cells (MCs) control the firing activity of the GC-BC loop by providing excitation to both the GCs and the BCs. SSR also appears in the population of MCs via interaction with the GCs (i.e., GC-MC loop). Population behaviors in the SSRs are quantitatively characterized in terms of the synchronization measures. In addition, we investigate individual firing activity of GCs, BCs, and MCs in the SSRs. Individual GCs exhibit random spike skipping, leading to a multi-peaked inter-spike-interval histogram, which is well characterized in terms of the random phase-locking degree. In this case, population-averaged mean-firing-rate (MFR) is less than the population frequency . On the other hand, both BCs and MCs show "intrastripe" burstings within stripes, together with random spike skipping. Thus, the population-averaged MFR ( MC and BC) is larger than , in contrast to the case of the GCs. MC loss may occur during epileptogenesis. With decreasing the fraction of the MCs, changes in the population and individual firings in the SSRs are also studied. Finally, quantitative association between the population/individual firing behaviors in the SSRs and the winner-take-all competition is discussed.

Behaviorally and environmentally induced non-24-hour sleep-wake rhythm disorder in sighted patients.

To determine whether there was evidence of circadian or sleep-regulatory dysfunction in sighted individuals with non-24-hour sleep-wake rhythm disorder. Three sighted individuals with signs and/or symptoms of non-24-hour sleep-wake rhythm disorder were studied. Thirty-five- to 332-day laboratory and home-based assessments of sleep-wake and circadian timing, endogenous circadian period, photic input to the circadian pacemaker, and/or circadian and sleep-wake-dependent regulation of sleep were conducted. No evidence of circadian dysfunction was found in these individuals. Instead, sleep-wake timing appeared to dissociate from the circadian timing system, and/or self-selected sleep-wake and associated light/dark timing shifted the circadian pacemaker later, rather than the circadian pacemaker determining sleep-wake timing. These findings suggest that the etiology of this disorder may be light- and/or behaviorally induced in some sighted people, which has implications for the successful treatment of this disorder. Emens JS, St Hilaire MA, Klerman EB, etal. Behaviorally and environmentally induced non-24-hour sleep-wake rhythm disorder in sighted patients. J Clin Sleep Med. 2022;18(2):453-459.

Region-specific Effects of Early-life Status Epilepticus on the Adult Hippocampal CA3 – Medial Entorhinal Cortex Circuitry In vitro: Focus on Interictal Spikes and Concurrent High-frequency Oscillations

Convulsive status epilepticus (SE) in immature life is often associated with lasting neurobiological changes. We provoked SE by pentylenetetrazole in postnatal day 20 rat pups and examined communication modalities between the temporal hippocampus and medial entorhinal cortex (mEC) in vitro. After a minimum of 40 days post-SE, we prepared combined temporal hippocampal – medial entorhinal cortex (mEC) slices from conditioned (SE) and naïve (N) adult rats and recorded 4-aminopyridine-induced spontaneous epileptiform interictal-like discharges (IED) simultaneously from CA3 and mEC layer V-VI. We analyzed IED frequency and high frequency oscillations (HFOs) in intact slices and after surgical separation of hippocampus from mEC, by two successive incisions (Schaffer collateral cut, Parasubiculum cut). In all slices, IED frequency was higher in CA3 vs mEC (5N, 4SE) and Raster plots indicated no temporal coincidence between them either in intact or in CA1-cut slices (4N, 4SE). IED frequency was significantly higher in SE mEC, but similar in SE and N CA3, independently of connectivity state. Ripples (R) and Fast Ripples (FR) coincided with IEDs and their power differed between SE and N intact slices (22N, 12SE), both in CA3 and mEC. CA3 FR/R ratios were higher in the absence of mEC (14N, 8SE). Moreover, SE (vs N) slices showed significantly higher FR/R ratios independently of the presence of mEC. Taken together, these findings suggest lasting effects of immature SE in network dynamics governing hippocampal-entorhinal communication which may impact adult cognitive, behavioral, and/or seizure threshold sequalae.

Collective Dynamics of Neural Networks With Sleep-Related Biological Drives in Drosophila.

The collective electrophysiological dynamics of the brain as a result of sleep-related biological drives in Drosophila are investigated in this paper. Based on the Huber-Braun thermoreceptor model, the conductance-based neurons model is extended to a coupled neural network to analyze the local field potential (LFP). The LFP is calculated by using two different metrics: the mean value and the distance-dependent LFP. The distribution of neurons around the electrodes is assumed to have a circular or grid distribution on a two-dimensional plane. Regardless of which method is used, qualitatively similar results are obtained that are roughly consistent with the experimental data. During wake, the LFP has an irregular or a regular spike. However, the LFP becomes regular bursting during sleep. To further analyze the results, wavelet analysis and raster plots are used to examine how the LFP frequencies changed. The synchronization of neurons under different network structures is also studied. The results demonstrate that there are obvious oscillations at approximately 8 Hz during sleep that are absent during wake. Different time series of the LFP can be obtained under different network structures and the density of the network will also affect the magnitude of the potential. As the number of coupled neurons increases, the neural network becomes easier to synchronize, but the sleep and wake time described by the LFP spectrogram do not change. Moreover, the parameters that affect the durations of sleep and wake are analyzed.

Study on propagation efficiency and fidelity of subthreshold signal in feed-forward hybrid neural network under electromagnetic radiation

The hybrid neural model provides a computationally effective and biophysics-based neuron behavior model, which maintains its simplicity by incorporating the dynamics characteristics of ion channels in two fast ion channels. In view of the issue of signal propagation in multilayer network composed of hybrid neurons is still unclear and the role of neural network is mainly used to generate biological consciousness and help creatures to think and act, it is necessary to explore neural network with more perfect function and better transmission efficiency. Considering a feed-forward neural network (FFN) which is composed of hybrid neurons in the presence of electromagnetic radiation, the effects of the Gaussian white noise, the strength of synaptic weight and inter-layer connection probability on subthreshold excitatory postsynaptic current (EPSC) propagation are investigated. In order to clarify the mechanism of signal transmission more clearly, the dot raster plot of spike and the corresponding post-spike time histogram of each layer are explored. Particularly, the propagation efficiency and fidelity of subthreshold EPSC signal in the FFN are investigated by calculating the power norm and the spike timing precision. Our results indicate that both the power norm and the spike timing precision fluctuate with the increase in the inter-layer connection probability, and the multi-periods bursting discharge mode can be detected in both the transmission layers and the output layer. Besides, there exists an optimal noise intensity to guarantee the best temporal coding and maximum transmission efficiency of subthreshold EPSC signal. Moreover, the optimal noise intensity makes the fidelity of the FFN the highest, which ensures that the weak signal and the excitation caused by noise can be distinguished. The conclusions obtained in this paper have potential value for discussing the encoding, decoding and propagation mechanism of information in real neural networks.

Symbolic analysis of bursting dynamical regimes of Rulkov neural networks

Neurons modeled by the Rulkov map display a variety of dynamic regimes that include tonic spikes and chaotic bursting. Here we study an ensemble of bursting neurons coupled with the Watts-Strogatz small-world topology. We characterize the sequences of bursts using the symbolic method of time-series analysis known as ordinal analysis, which detects nonlinear temporal correlations. We show that the probabilities of the different symbols distinguish different dynamical regimes, which depend on the coupling strength and the network topology. These regimes have different spatio-temporal properties that can be visualized with raster plots.

Three-dimensional imaging and quantification of real-time cytosolic calcium oscillations in microglial cells cultured on electrospun matrices using laser scanning confocal microscopy.

The development of a minimally invasive, robust, and inexpensive technique that permits real-time monitoring of cell responses on biomaterial scaffolds can improve the eventual outcomes of scaffold-based tissue engineering strategies. Towards establishing correlations between in situ biological activity and cell fate, we have developed a comprehensive workflow for real-time volumetric imaging of spatiotemporally varying cytosolic calcium oscillations in pure microglial cells cultured on electrospun meshes. Live HMC3 cells on randomly oriented electrospun fibers were stained with a fluorescent dye and imaged using a laser scanning confocal microscope. Resonance scanning provided high-resolution in obtaining the time-course of intracellular calcium levels without compromising spatial and temporal resolution. Three-dimensional reconstruction and depth-coding enabled the visualization of cell location and intracellular calcium levels as a function of sample thickness. Importantly, changes in cell morphology and in situ calcium spiking were quantified in response to a soluble biochemical cue and varying matrix architectures (i.e., randomly oriented and aligned fibers). Importantly, raster plots generated from spiking data revealed calcium signatures specific to culture conditions. In the future, our approach can be used to elucidate correlations between calcium signatures and cell phenotype/activation, and facilitate the rational design of scaffolds for biomedical applications.

Spikes and Nets (S&N): A New Fast, Parallel Computing, Point Process Software for Multineuronal Discharge and Connectivity Analysis

SN however, the aim of this work was to develop an easy to use, fast, short learning curve, multi-platform and parallel computing software able to manage a large number of neuronal spike train files to detect discharge patterns, connectivity, and time-dependent changes. A set of the most used spike train methods to perform single and multi-neuronal discharge pattern recognition and functional connectivity analysis were implemented in an easy-to-use, standalone, Matlab-based software toolbox: spikes and nets (S&N). The methods included for single and multi-neuronal discharge pattern analysis are raster plot, interspike intervals distribution, multiparametric burst, auto-correlation, auto-spectral, fractal, poincare, and phases. For functional connectivity analysis, cross-correlation and joint interval scatter diagram were implemented. Additionally, time segmentation analysis is available to detect temporal changes for all methods. S&N efficiently handles large numbers of neuronal discharge files at once with fast and automatic archiving of both analytical and graphical results which makes it suitable for multi-electrode array data. S&N applies up to 11 different analytical methods, including automatic file segmentation for time-dependent changes detection, and generates publication quality graphs. The developed toolbox is multi-platform and reads universal spike train files with any temporal resolution, able to process also ECG, EEG or similar data files.

Analog Complementary Metal-Oxide-Semiconductor Integrate-and-Fire Neuron Circuit for Overflow Retaining in Hardware Spiking Neural Networks.

The spiking neural network (SNN) is regarded as the third generation of an artificial neural network (ANN). In order to realize a high-performance SNN, an integrate-and-fire (I&F) neuron, one of the key elements in an SNN, must retain the overflow in its membrane after firing. This paper presents an analog CMOS I&F neuron circuit for overflow retaining. Compared with the conventional I&F neuron circuit, the basic operation of the proposed circuit is confirmed in a circuit-level simulation. Furthermore, a single-layer SNN simulation was also performed to demonstrate the effect of the proposed circuit on neural network applications by comparing the raster plots from the circuit-level simulation with those from a high-level simulation. These results demonstrate the potential of the I&F neuron circuit with overflow retaining characteristics to be utilized in upcoming high-performance hardware SNN systems.

Effect of interpopulation spike-timing-dependent plasticity on synchronized rhythms in neuronal networks with inhibitory and excitatory populations.

We consider a two-population network consisting of both inhibitory (I) interneurons and excitatory (E) pyramidal cells. This I-E neuronal network has adaptive dynamic I to E and E to I interpopulation synaptic strengths, governed by interpopulation spike-timing-dependent plasticity (STDP). In previous works without STDPs, fast sparsely synchronized rhythms, related to diverse cognitive functions, were found to appear in a range of noise intensity D for static synaptic strengths. Here, by varying D, we investigate the effect of interpopulation STDPs on fast sparsely synchronized rhythms that emerge in both the I- and the E-populations. Depending on values of D, long-term potentiation (LTP) and long-term depression (LTD) for population-averaged values of saturated interpopulation synaptic strengths are found to occur. Then, the degree of fast sparse synchronization varies due to effects of LTP and LTD. In a broad region of intermediate D, the degree of good synchronization (with higher synchronization degree) becomes decreased, while in a region of large D, the degree of bad synchronization (with lower synchronization degree) gets increased. Consequently, in each I- or E-population, the synchronization degree becomes nearly the same in a wide range of D (including both the intermediate and the large D regions). This kind of "equalization effect" is found to occur via cooperative interplay between the average occupation and pacing degrees of spikes (i.e., the average fraction of firing neurons and the average degree of phase coherence between spikes in each synchronized stripe of spikes in the raster plot of spikes) in fast sparsely synchronized rhythms. Finally, emergences of LTP and LTD of interpopulation synaptic strengths (leading to occurrence of equalization effect) are intensively investigated via a microscopic method based on the distributions of time delays between the pre- and the post-synaptic spike times.

Cluster burst synchronization in a scale-free network of inhibitory bursting neurons.

We consider a scale-free network of inhibitory Hindmarsh-Rose (HR) bursting neurons, and make a computational study on coupling-induced cluster burst synchronization by varying the average coupling strength . For sufficiently small , non-cluster desynchronized states exist. However, when passing a critical point , the whole population is segregated into 3 clusters via a constructive role of synaptic inhibition to stimulate dynamical clustering between individual burstings, and thus 3-cluster desynchronized states appear. As is further increased and passes a lower threshold , a transition to 3-cluster burst synchronization occurs due to another constructive role of synaptic inhibition to favor population synchronization. In this case, HR neurons in each cluster make burstings every 3rd cycle of the instantaneous burst rate of the whole population, and exhibit burst synchronization. However, as passes an intermediate threshold , HR neurons fire burstings intermittently at a 4th cycle of via burst skipping rather than at its 3rd cycle, and hence they begin to make intermittent hoppings between the 3 clusters. Due to such intermittent intercluster hoppings via burst skippings, the 3 clusters become broken up (i.e., the 3 clusters are integrated into a single one). However, in spite of such break-up (i.e., disappearance) of the 3-cluster states, (non-cluster) burst synchronization persists in the whole population, which is well visualized in the raster plot of burst onset times where bursting stripes (composed of burst onset times and indicating burst synchronization) appear successively. With further increase in , intercluster hoppings are intensified, and bursting stripes also become dispersed more and more due to a destructive role of synaptic inhibition to spoil the burst synchronization. Eventually, when passing a higher threshold a transition to desynchronization occurs via complete overlap between the bursting stripes. Finally, we also investigate the effects of stochastic noise on both 3-cluster burst synchronization and intercluster hoppings.

Self-Organized Synchronous Calcium Transients in a Cultured Human Neural Network Derived from Cerebral Organoids.

SummaryThe cerebrum is a major center for brain function, and its activity is derived from the assembly of activated cells in neural networks. It is currently difficult to study complex human cerebral neuronal network activity. Here, using cerebral organoids, we report self-organized and complex human neural network activities that include synchronized and non-synchronized patterns. Self-organized neuronal network formation was observed following a dissociation culture of human embryonic stem cell-derived cerebral organoids. The spontaneous individual and synchronized activity of the network was measured via calcium imaging, and subsequent analysis enabled the examination of detailed cell activity patterns, providing simultaneous raster plots, cluster analyses, and cell distribution data. Finally, we demonstrated the feasibility of our system to assess drug-inducible dynamic changes of the network activity. The comprehensive functional analysis of human neuronal networks using this system may offer a powerful tool to access human brain function.

A design of raster plot for illustrating dynamic neuronal activity during deep brain stimulation

Deep brain stimulation (DBS), which usually utilizes high frequency stimulation (HFS) of electrical pulses, is effective for treating many brain disorders in clinic. Studying the dynamic response of downstream neurons to HFS and its time relationship with stimulus pulses can reveal important mechanisms of DBS and advance the development of new stimulation modes (e.g., closed-loop DBS). To exhibit the dynamic neuronal firing and its relationship with stimuli, we designed a two-dimensional raster plot to visualize neuronal activity during HFS (especially in the initial stage of HFS). Additionally, the influence of plot resolution on the visualization effect was investigated. The method was then validated by investigating the neuronal responses to the axonal HFS in the hippocampal CA1 region of rats. Results show that the new design of raster plot is able to illustrate the dynamics of indexes (such as phase-locked relationship and latency) of single unit activity (i.e., spikes) during periodic pulse stimulations. Furthermore, the plots can intuitively show changes of neuronal firing from the baseline before stimulation to the onset dynamics during stimulation, as well as other information including the silent period of spikes immediately following the end of HFS. In addition, by adjusting resolution, the raster plot can be adapted to a large range of firing rates for clear illustration of neuronal activity. The new raster plot can illustrate more information with a clearer image than a regular raster plot, and thereby provides a useful tool for studying neuronal behaviors during high-frequency stimulations in brain.

Stochastic oscillations and dragon king avalanches in self-organized quasi-critical systems

In the last decade, several models with network adaptive mechanisms (link deletion-creation, dynamic synapses, dynamic gains) have been proposed as examples of self-organized criticality (SOC) to explain neuronal avalanches. However, all these systems present stochastic oscillations hovering around the critical region that are incompatible with standard SOC. Here we make a linear stability analysis of the mean field fixed points of two self-organized quasi-critical systems: a fully connected network of discrete time stochastic spiking neurons with firing rate adaptation produced by dynamic neuronal gains and an excitable cellular automata with depressing synapses. We find that the fixed point corresponds to a stable focus that loses stability at criticality. We argue that when this focus is close to become indifferent, demographic noise can elicit stochastic oscillations that frequently fall into the absorbing state. This mechanism interrupts the oscillations, producing both power law avalanches and dragon king events, which appear as bands of synchronized firings in raster plots. Our approach differs from standard SOC models in that it predicts the coexistence of these different types of neuronal activity.