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Eric Shea-Brown

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Published work

31 published item(s)

preprint2026arXiv

State-Space NTK Collapse Near Bifurcations

Rich feature learning in tasks that unfold over time often requires the model to pass through bifurcations, constituting qualitative changes in the underlying model dynamics. We develop a local theory of gradient descent near these transitions through the empirical state-space neural tangent kernel (sNTK). Our central finding is that bifurcations both dominate and simplify learning dynamics: near bifurcations, we can reduce sNTK to a rank-one operator corresponding to learning in a classical normal form system, providing an analytically tractable description of the local learning geometry, even for high-dimensional recurrent systems. Concretely, we give a procedure for decomposing sNTK into bifurcation-relevant and residual channels, showing that near commonly codimension-1 bifurcations the relevant channel is a rank-one operator that is highly amplified. This amplification causes the bifurcation channel to dominate the full sNTK. Thus, bifurcations locally warp the learning landscape, funneling gradient descent into a few critical dynamical directions and making the nearby kernel and loss geometry predictable from classical normal forms. We illustrate this in a student-teacher recurrent neural network: the first learned bifurcation coincides with a sharp collapse in sNTK effective rank and the emergence of a dominant parameter direction whose restricted sNTK closely matches the landscape predicted by the scalar pitchfork normal form. Finally, we show that low-rank natural gradient methods resolve the resulting learning instability near bifurcations with very little overhead over SGD.

preprint2026arXiv

The Global Empirical NTK: Self-Referential Bias and Dimensionality of Gradient Descent Learning

In training a neural network with gradient descent (GD), each iteration induces a linear operator that governs first-order updates to a model's internal state variables. We define this operator as the Global Empirical Neural Tangent Kernel (NTK). In finite-width networks, the NTK is typically intractable to form, leading prior work to focus on restrictive settings such as tracking outputs only or taking infinite-width limits. Here, we study the structure of the NTK for a range of models. Formulating the model state as the solution to a single global implicit constraint, we derive the NTK as a product of two operators: K, accounting for immediate parameter-to-state interactions, and P, describing internal state-to-state dependencies. For a broad class of weight-based models, including RNNs and transformers, we prove a universal Kronecker-core theorem showing that K admits an exact, computable form given by the Gram matrix of weight-site variables. This core structure reveals that the NTK is structurally bottlenecked, constraining its effective rank and giving rise to a self-referential bias whereby GD preferentially learns within dominant modes of joint hidden and input activity. For recurrent models, we examine the spectrum of the NTK and show when it is biased and low-rank in space or time under the proposed decomposition. We further demonstrate that model dynamics at initialization bias the NTK, restricting learning and preventing task components from being learned effectively. Finally, we show that the NTK associated with a self-attention transformer is likewise structurally constrained to be low-rank. Overall, we show that the NTK possesses tractable structure that explains GD bias toward task solutions and the emergence of low-rank representations. To enable use of the NTK as a practical metric, we build kpflow, a library relying on randomized matrix-free numerical linear algebra.

preprint2023arXiv

Beyond accuracy: generalization properties of bio-plausible temporal credit assignment rules

To unveil how the brain learns, ongoing work seeks biologically-plausible approximations of gradient descent algorithms for training recurrent neural networks (RNNs). Yet, beyond task accuracy, it is unclear if such learning rules converge to solutions that exhibit different levels of generalization than their nonbiologically-plausible counterparts. Leveraging results from deep learning theory based on loss landscape curvature, we ask: how do biologically-plausible gradient approximations affect generalization? We first demonstrate that state-of-the-art biologically-plausible learning rules for training RNNs exhibit worse and more variable generalization performance compared to their machine learning counterparts that follow the true gradient more closely. Next, we verify that such generalization performance is correlated significantly with loss landscape curvature, and we show that biologically-plausible learning rules tend to approach high-curvature regions in synaptic weight space. Using tools from dynamical systems, we derive theoretical arguments and present a theorem explaining this phenomenon. This predicts our numerical results, and explains why biologically-plausible rules lead to worse and more variable generalization properties. Finally, we suggest potential remedies that could be used by the brain to mitigate this effect. To our knowledge, our analysis is the first to identify the reason for this generalization gap between artificial and biologically-plausible learning rules, which can help guide future investigations into how the brain learns solutions that generalize.

preprint2023arXiv

Biologically-plausible backpropagation through arbitrary timespans via local neuromodulators

The spectacular successes of recurrent neural network models where key parameters are adjusted via backpropagation-based gradient descent have inspired much thought as to how biological neuronal networks might solve the corresponding synaptic credit assignment problem. There is so far little agreement, however, as to how biological networks could implement the necessary backpropagation through time, given widely recognized constraints of biological synaptic network signaling architectures. Here, we propose that extra-synaptic diffusion of local neuromodulators such as neuropeptides may afford an effective mode of backpropagation lying within the bounds of biological plausibility. Going beyond existing temporal truncation-based gradient approximations, our approximate gradient-based update rule, ModProp, propagates credit information through arbitrary time steps. ModProp suggests that modulatory signals can act on receiving cells by convolving their eligibility traces via causal, time-invariant and synapse-type-specific filter taps. Our mathematical analysis of ModProp learning, together with simulation results on benchmark temporal tasks, demonstrate the advantage of ModProp over existing biologically-plausible temporal credit assignment rules. These results suggest a potential neuronal mechanism for signaling credit information related to recurrent interactions over a longer time horizon. Finally, we derive an in-silico implementation of ModProp that could serve as a low-complexity and causal alternative to backpropagation through time.

preprint2020arXiv

Firing rate of the leaky integrate-and-fire neuron with stochastic conductance-based synaptic inputs with short decay times

We compute the firing rate of a leaky integrate-and-fire (LIF) neuron with stochastic conductance-based inputs in the limit when synaptic decay times are much shorter than the membrane time constant. A comparison of our analytical results to numeric simulations is presented for a range of biophysically-realistic parameters.

preprint2020arXiv

Linking structure and activity in nonlinear spiking networks

Recent experimental advances are producing an avalanche of data on both neural connectivity and neural activity. To take full advantage of these two emerging datasets we need a framework that links them, revealing how collective neural activity arises from the structure of neural connectivity and intrinsic neural dynamics. This problem of {\it structure-driven activity} has drawn major interest in computational neuroscience. Existing methods for relating activity and architecture in spiking networks rely on linearizing activity around a central operating point and thus fail to capture the nonlinear responses of individual neurons that are the hallmark of neural information processing. Here, we overcome this limitation and present a new relationship between connectivity and activity in networks of nonlinear spiking neurons by developing a diagrammatic fluctuation expansion based on statistical field theory. We explicitly show how recurrent network structure produces pairwise and higher-order correlated activity, and how nonlinearities impact the networks' spiking activity. Our findings open new avenues to investigating how single-neuron nonlinearities---including those of different cell types---combine with connectivity to shape population activity and function.

preprint2020arXiv

Network Dynamics Governed by Lyapunov Functions: From Memory to Classification

In 1982 John Hopfield published a neural network model for memory retrieval, a model that became a cornerstone in theoretical neuroscience. A key ingredient of the Hopfield model was the use of a network dynamics that is governed by a Lyapunov function. In a recent paper, Krotov and Hopfield showed how a Lyapunov function governs a biological plausible learning rule for the neural networks' connectivity. By doing so, they bring an intriguing approach to classification tasks, and show the relevance of the broader framework across decades in the field.

preprint2016arXiv

High resolution neural connectivity from incomplete tracing data using nonnegative spline regression

Whole-brain neural connectivity data are now available from viral tracing experiments, which reveal the connections between a source injection site and elsewhere in the brain. These hold the promise of revealing spatial patterns of connectivity throughout the mammalian brain. To achieve this goal, we seek to fit a weighted, nonnegative adjacency matrix among 100 $μ$m brain "voxels" using viral tracer data. Despite a multi-year experimental effort, injections provide incomplete coverage, and the number of voxels in our data is orders of magnitude larger than the number of injections, making the problem severely underdetermined. Furthermore, projection data are missing within the injection site because local connections there are not separable from the injection signal. We use a novel machine-learning algorithm to meet these challenges and develop a spatially explicit, voxel-scale connectivity map of the mouse visual system. Our method combines three features: a matrix completion loss for missing data, a smoothing spline penalty to regularize the problem, and (optionally) a low rank factorization. We demonstrate the consistency of our estimator using synthetic data and then apply it to newly available Allen Mouse Brain Connectivity Atlas data for the visual system. Our algorithm is significantly more predictive than current state of the art approaches which assume regions to be homogeneous. We demonstrate the efficacy of a low rank version on visual cortex data and discuss the possibility of extending this to a whole-brain connectivity matrix at the voxel scale.

preprint2016arXiv

Predictive coding in area V4: dynamic shape discrimination under partial occlusion

The primate visual system has an exquisite ability to discriminate partially occluded shapes. Recent electrophysiological recordings suggest that response dynamics in intermediate visual cortical area V4, shaped by feedback from prefrontal cortex (PFC), may play a key role. To probe the algorithms that may underlie these findings, we build and test a model of V4 and PFC interactions based on a hierarchical predictive coding framework. We propose that probabilistic inference occurs in two steps. Initially, V4 responses are driven solely by bottom-up sensory input and are thus strongly influenced by the level of occlusion. After a delay, V4 responses combine both feedforward input and feedback signals from the PFC; the latter reflect predictions made by PFC about the visual stimulus underlying V4 activity. We find that this model captures key features of V4 and PFC dynamics observed in experiments. Specifically, PFC responses are strongest for occluded stimuli and delayed responses in V4 are less sensitive to occlusion, supporting our hypothesis that the feedback signals from PFC underlie robust discrimination of occluded shapes. Thus, our study proposes that area V4 and PFC participate in hierarchical inference, with feedback signals encoding top-down predictions about occluded shapes.

preprint2016arXiv

Revisiting chaos in stimulus-driven spiking networks: signal encoding and discrimination

Highly connected recurrent neural networks often produce chaotic dynamics, meaning their precise activity is sensitive to small perturbations. What are the consequences for how such networks encode streams of temporal stimuli? On the one hand, chaos is a strong source of randomness, suggesting that small changes in stimuli will be obscured by intrinsically generated variability. On the other hand, recent work shows that the type of chaos that occurs in spiking networks can have a surprisingly low-dimensional structure, suggesting that there may be "room" for fine stimulus features to be precisely resolved. Here we show that strongly chaotic networks produce patterned spikes that reliably encode time-dependent stimuli: using a decoder sensitive to spike times on timescales of 10's of ms, one can easily distinguish responses to very similar inputs. Moreover, recurrence serves to distribute signals throughout chaotic networks so that small groups of cells can encode substantial information about signals arriving elsewhere. A conclusion is that the presence of strong chaos in recurrent networks does not prohibit precise stimulus encoding.

preprint2015arXiv

Input nonlinearities can shape beyond-pairwise correlations and improve information transmission by neural populations

While recent recordings from neural populations show beyond-pairwise, or higher-order correlations (HOC), we have little understanding of how HOC arise from network interactions and of how they impact encoded information. Here, we show that input nonlinearities imply HOC in spin-glass-type statistical models. We then discuss one such model with parameterized pairwise- and higher-order interactions, revealing conditions under which beyond-pairwise interactions increase the mutual information between a given stimulus type and the population responses. For jointly Gaussian stimuli, coding performance is improved by shaping output HOC only when neural firing rates are constrained to be low. For stimuli with skewed probability distributions (like natural image luminances), performance improves for all firing rates. Our work suggests surprising connections between nonlinear integration of neural inputs, stimulus statistics, and normative theories of population coding. Moreover, it suggests that the inclusion of beyond-pairwise interactions could improve the performance of Boltzmann machines for machine learning and signal processing applications.

preprint2014arXiv

Impact of triplet correlations on neural population codes

Which statistical features of spiking activity matter for how stimuli are encoded in neural populations? A vast body of work has explored how firing rates in individual cells and correlations in the spikes of cell pairs impact coding. But little is known about how higher-order correlations, which describe simultaneous firing in triplets and larger ensembles of cells, impact encoded stimulus information. Here, we take a first step toward closing this gap. We vary triplet correlations in small (~10 cell) neural populations while keeping single cell and pairwise statistics fixed at typically reported values. For each value of triplet correlations, we estimate the performance of the neural population on a two-stimulus discrimination task. We identify a predominant way that such triplet correlations can strongly enhance coding: if triplet correlations differ for the two stimuli, they skew the response distributions of the two stimuli apart from each other, separating them and making them easier to distinguish. This coding benefit does not occur when both stimuli elicit similar triplet correlations. These results indicate that higher-order correlations could have a strong effect on population coding. Finally, we calculate how many samples are necessary to accurately measure spiking correlations of this type, providing an estimate of the necessary recording times in experiments.

preprint2014arXiv

Structured chaos shapes spike-response noise entropy in balanced neural networks

Large networks of sparsely coupled, excitatory and inhibitory cells occur throughout the brain. A striking feature of these networks is that they are chaotic. How does this chaos manifest in the neural code? Specifically, how variable are the spike patterns that such a network produces in response to an input signal? To answer this, we derive a bound for the entropy of multi-cell spike pattern distributions in large recurrent networks of spiking neurons responding to fluctuating inputs. The analysis is based on results from random dynamical systems theory and is complimented by detailed numerical simulations. We find that the spike pattern entropy is an order of magnitude lower than what would be extrapolated from single cells. This holds despite the fact that network coupling becomes vanishingly sparse as network size grows -- a phenomenon that depends on ``extensive chaos," as previously discovered for balanced networks without stimulus drive. Moreover, we show how spike pattern entropy is controlled by temporal features of the inputs. Our findings provide insight into how neural networks may encode stimuli in the presence of inherently chaotic dynamics.

preprint2014arXiv

The sign rule and beyond: Boundary effects, flexibility, and noise correlations in neural population codes

Over repeat presentations of the same stimulus, sensory neurons show variable responses. This "noise" is typically correlated between pairs of cells, and a question with rich history in neuroscience is how these noise correlations impact the population's ability to encode the stimulus. Here, we consider a very general setting for population coding, investigating how information varies as a function of noise correlations, with all other aspects of the problem - neural tuning curves, etc. - held fixed. This work yields unifying insights into the role of noise correlations. These are summarized in the form of theorems, and illustrated with numerical examples involving neurons with diverse tuning curves. Our main contributions are as follows. (1) We generalize previous results to prove a sign rule (SR) - if noise correlations between pairs of neurons have opposite signs vs. their signal correlations, then coding performance will improve compared to the independent case. This holds for three different metrics of coding performance, and for arbitrary tuning curves and levels of heterogeneity. This generality is true for our other results as well. (2) As also pointed out in the literature, the SR does not provide a necessary condition for good coding. We show that a diverse set of correlation structures can improve coding. Many of these violate the SR, as do experimentally observed correlations. There is structure to this diversity: we prove that the optimal correlation structures must lie on boundaries of the possible set of noise correlations. (3) We provide a novel set of necessary and sufficient conditions, under which the coding performance (in the presence of noise) will be as good as it would be if there were no noise present at all.

preprint2013arXiv

A generative spike train model with time-structured higher order correlations

Emerging technologies are revealing the spiking activity in ever larger neural ensembles. Frequently, this spiking is far from independent, with correlations in the spike times of different cells. Understanding how such correlations impact the dynamics and function of neural ensembles remains an important open problem. Here we describe a new, generative model for correlated spike trains that can exhibit many of the features observed in data. Extending prior work in mathematical finance, this generalized thinning and shift (GTaS) model creates marginally Poisson spike trains with diverse temporal correlation structures. We give several examples which highlight the model's flexibility and utility. For instance, we use it to examine how a neural network responds to highly structured patterns of inputs. We then show that the GTaS model is analytically tractable, and derive cumulant densities of all orders in terms of model parameters. The GTaS framework can therefore be an important tool in the experimental and theoretical exploration of neural dynamics.

preprint2013arXiv

A simple mechanism for higher-order correlations in integrate-and-fire neurons

The collective dynamics of neural populations are often characterized in terms of correlations in the spike activity of different neurons. Open questions surround the basic nature of these correlations. In particular, what leads to higher-order correlations -- correlations in the population activity that extend beyond those expected from cell pairs? Here, we examine this question for a simple, but ubiquitous, circuit feature: common fluctuating input arriving to spiking neurons of integrate-and-fire type. We show that leads to strong higher-order correlations, as for earlier work with discrete threshold crossing models. Moreover, we find that the same is true for another widely used, doubly-stochastic model of neural spiking, the linear-nonlinear cascade. We explain the surprisingly strong connection between the collective dynamics produced by these models, and conclude that higher-order correlations are both broadly expected and possible to capture with surprising accuracy by simplified (and tractable) descriptions of neural spiking.

preprint2013arXiv

Chaos and reliability in balanced spiking networks with temporal drive

Biological information processing is often carried out by complex networks of interconnected dynamical units. A basic question about such networks is that of reliability: if the same signal is presented many times with the network in different initial states, will the system entrain to the signal in a repeatable way? Reliability is of particular interest in neuroscience, where large, complex networks of excitatory and inhibitory cells are ubiquitous. These networks are known to autonomously produce strongly chaotic dynamics - an obvious threat to reliability. Here, we show that such chaos persists in the presence of weak and strong stimuli, but that even in the presence of chaos, intermittent periods of highly reliable spiking often coexist with unreliable activity. We elucidate the local dynamical mechanisms involved in this intermittent reliability, and investigate the relationship between this phenomenon and certain time-dependent attractors arising from the dynamics. A conclusion is that chaotic dynamics do not have to be an obstacle to precise spike responses, a fact with implications for signal coding in large networks.

preprint2013arXiv

Local paths to global coherence: cutting networks down to size

How does connectivity impact network dynamics? We address this question by linking network characteristics on two scales. On the global scale we consider the coherence of overall network dynamics. We show that such \emph{global coherence} in activity can often be predicted from the \emph{local structure} of the network. To characterize local network structure we use "motif cumulants," a measure of the deviation of pathway counts from those expected in a minimal probabilistic network model. We extend previous results in three ways. First, we give a new combinatorial formulation of motif cumulants that relates to the allied concept in probability theory. Second, we show that the link between global network dynamics and local network architecture is strongly affected by heterogeneity in network connectivity. However, we introduce a network-partitioning method that recovers a tight relationship between architecture and dynamics. Third, for a particular set of models we generalize the underlying theory to treat dynamical coherence at arbitrary orders (i.e. triplet correlations, and beyond). We show that at any order only a highly restricted set of motifs impact dynamical correlations.

preprint2012arXiv

A point process framework for modeling electrical stimulation of the auditory nerve

Model-based studies of auditory nerve responses to electrical stimulation can provide insight into the functioning of cochlear implants. Ideally, these studies can identify limitations in sound processing strategies and lead to improved methods for providing sound information to cochlear implant users. To accomplish this, models must accurately describe auditory nerve spiking while avoiding excessive complexity that would preclude large-scale simulations of populations of auditory nerve fibers and obscure insight into the mechanisms that influence neural encoding of sound information. In this spirit, we develop a point process model of the auditory nerve that provides a compact and accurate description of neural responses to electric stimulation. Inspired by the framework of generalized linear models, the proposed model consists of a cascade of linear and nonlinear stages. We show how each of these stages can be associated with biophysical mechanisms and related to models of neuronal dynamics. Moreover, we derive a semi-analytical procedure that uniquely determines each parameter in the model on the basis of fundamental statistics from recordings of single fiber responses to electric stimulation, including threshold, relative spread, jitter, and chronaxie. The model also accounts for refractory and summation effects that influence the responses of auditory nerve fibers to high pulse rate stimulation. Throughout, we compare model predictions to published physiological data and explain differences in auditory nerve responses to high and low pulse rate stimulation. We close by performing an ideal observer analysis of simulated spike trains in response to sinusoidally amplitude modulated stimuli and find that carrier pulse rate does not affect modulation detection thresholds.

preprint2012arXiv

Impact of correlated neural activity on decision making performance

Stimulus from the environment that guides behavior and informs decisions is encoded in the firing rates of neural populations. Each neuron in the populations, however, does not spike independently: spike events are correlated from cell to cell. To what degree does this apparent redundancy impact the accuracy with which decisions can be made, and the computations that are required to optimally decide? We explore these questions for two illustrative models of correlation among cells. Each model is statistically identical at the level of pairs cells, but differs in higher-order statistics that describe the simultaneous activity of larger cell groups. We find that the presence of correlations can diminish the performance attained by an ideal decision maker to either a small or large extent, depending on the nature of the higher-order interactions. Moreover, while this optimal performance can in some cases be obtained via the standard integration-to-bound operation, in others it requires a nonlinear computation on incoming spikes. Overall, we conclude that a given level of pairwise correlations--even when restricted to identical neural populations--may not always indicate redundancies that diminish decision making performance.

preprint2012arXiv

Motif Statistics and Spike Correlations in Neuronal Networks

Motifs are patterns of subgraphs of complex networks. We studied the impact of such patterns of connectivity on the level of correlated, or synchronized, spiking activity among pairs of cells in a recurrent network model of integrate and fire neurons. For a range of network architectures, we find that the pairwise correlation coefficients, averaged across the network, can be closely approximated using only three statistics of network connectivity. These are the overall network connection probability and the frequencies of two second-order motifs: diverging motifs, in which one cell provides input to two others, and chain motifs, in which two cells are connected via a third intermediary cell. Specifically, the prevalence of diverging and chain motifs tends to increase correlation. Our method is based on linear response theory, which enables us to express spiking statistics using linear algebra, and a resumming technique, which extrapolates from second order motifs to predict the overall effect of coupling on network correlation. Our motif-based results seek to isolate the effect of network architecture perturbatively from a known network state.

preprint2012arXiv

Neutral stability, rate propagation, and critical branching in feedforward networks

Recent experimental and computational evidence suggests that several dynamical properties may characterize the operating point of functioning neural networks: critical branching, neutral stability, and production of a wide range of firing patterns. We seek the simplest setting in which these properties emerge, clarifying their origin and relationship in random, feedforward networks of McCullochs-Pitts neurons. Two key parameters are the thresholds at which neurons fire spikes, and the overall level of feedforward connectivity. When neurons have low thresholds, we show that there is always a connectivity for which the properties in question all occur: that is, these networks preserve overall firing rates from layer to layer and produce broad distributions of activity in each layer. This fails to occur, however, when neurons have high thresholds. A key tool in explaining this difference is eigenstructure of the resulting mean-field Markov chain, as this reveals which activity modes will be preserved from layer to layer. We extend our analysis from purely excitatory networks to more complex models that include inhibition and 'local' noise, and find that both of these features extend the parameter ranges over which networks produce the properties of interest.

preprint2012arXiv

When are microcircuits well-modeled by maximum entropy methods?

Describing the collective activity of neural populations is a daunting task: the number of possible patterns grows exponentially with the number of cells, resulting in practically unlimited complexity. Recent empirical studies, however, suggest a vast simplification in how multi-neuron spiking occurs: the activity patterns of some circuits are nearly completely captured by pairwise interactions among neurons. Why are such pairwise models so successful in some instances, but insufficient in others? Here, we study the emergence of higher-order interactions in simple circuits with different architectures and inputs. We quantify the impact of higher-order interactions by comparing the responses of mechanistic circuit models vs. "null" descriptions in which all higher-than-pairwise correlations have been accounted for by lower order statistics, known as pairwise maximum entropy models. We find that bimodal input signals produce larger deviations from pairwise predictions than unimodal inputs for circuits with local and global connectivity. Moreover, recurrent coupling can accentuate these deviations, if coupling strengths are neither too weak nor too strong. A circuit model based on intracellular recordings from ON parasol retinal ganglion cells shows that a broad range of light signals induce unimodal inputs to spike generators, and that coupling strengths produce weak effects on higher-order interactions. This provides a novel explanation for the success of pairwise models in this system. Overall, our findings identify circuit-level mechanisms that produce and fail to produce higher-order spiking statistics in neural ensembles.

preprint2011arXiv

Impact of network structure and cellular response on spike time correlations

Novel experimental techniques reveal the simultaneous activity of larger and larger numbers of neurons. As a result there is increasing interest in the structure of cooperative -- or correlated -- activity in neural populations, and in the possible impact of such correlations on the neural code. A fundamental theoretical challenge is to understand how the architecture of network connectivity along with the dynamical properties of single cells shape the magnitude and timescale of correlations. We provide a general approach to this problem by extending prior techniques based on linear response theory. We consider networks of general integrate-and-fire cells with arbitrary architecture, and provide explicit expressions for the approximate cross-correlation between constituent cells. These correlations depend strongly on the operating point (input mean and variance) of the neurons, even when connectivity is fixed. Moreover, the approximations admit an expansion in powers of the matrices that describe the network architecture. This expansion can be readily interpreted in terms of paths between different cells. We apply our results to large excitatory-inhibitory networks, and demonstrate first how precise balance --- or lack thereof --- between the strengths and timescales of excitatory and inhibitory synapses is reflected in the overall correlation structure of the network. We then derive explicit expressions for the average correlation structure in randomly connected networks. These expressions help to identify the important factors that shape coordinated neural activity in such networks.

preprint2011arXiv

Neural integrators for decision making: A favorable tradeoff between robustness and sensitivity

A key step in many perceptual decision tasks is the integration of sensory inputs over time, but fundamental questions remain about how this is accomplished in neural circuits. One possibility is to balance decay modes of membranes and synapses with recurrent excitation. To allow integration over long timescales, however, this balance must be precise; this is known as the fine tuning problem. The need for fine tuning can be overcome via a ratchet-like mechanism, in which momentary inputs must be above a preset limit to be registered by the circuit. The degree of this ratcheting embodies a tradeoff between sensitivity to the input stream and robustness against parameter mistuning. The goal of our study is to analyze the consequences of this tradeoff for decision making performance. For concreteness, we focus on the well-studied random dot motion discrimination task. For stimulus parameters constrained by experimental data, we find that loss of sensitivity to inputs has surprisingly little cost for decision performance. This leads robust integrators to performance gains when feedback becomes mistuned. Moreover, we find that substantially robust and mistuned integrator models remain consistent with chronometric and accuracy functions found in experiments. We explain our findings via sequential analysis of the momentary and integrated signals, and discuss their implication: robust integrators may be surprisingly well-suited to subserve the basic function of evidence integration in many cognitive tasks.

preprint2011arXiv

Shared inputs, entrainment, and desynchrony in elliptic bursters: from slow passage to discontinuous circle maps

What input signals will lead to synchrony vs. desynchrony in a group of biological oscillators? This question connects with both classical dynamical systems analyses of entrainment and phase locking and with emerging studies of stimulation patterns for controlling neural network activity. Here, we focus on the response of a population of uncoupled, elliptically bursting neurons to a common pulsatile input. We extend a phase reduction from the literature to capture inputs of varied strength, leading to a circle map with discontinuities of various orders. In a combined analytical and numerical approach, we apply our results to both a normal form model for elliptic bursting and to a biophysically-based neuron model from the basal ganglia. We find that, depending on the period and amplitude of inputs, the response can either appear chaotic (with provably positive Lyaponov exponent for the associated circle maps), or periodic with a broad range of phase-locked periods. Throughout, we discuss the critical underlying mechanisms, including slow-passage effects through Hopf bifurcation, the role and origin of discontinuities, and the impact of noise

preprint2011arXiv

The A-current and Type I / Type II transition determine collective spiking from common input

The mechanisms and impact of correlated, or synchronous, firing among pairs and groups of neurons is under intense investigation throughout the nervous system. A ubiquitous circuit feature that can give rise to such correlations consists of overlapping, or common, inputs to pairs and populations of cells, leading to common spike train responses. Here, we use computational tools to study how the transfer of common input currents into common spike outputs is modulated by the physiology of the recipient cells. We focus on a key conductance - gA, for the A-type potassium current - which drives neurons between "Type II" excitability (low gA), and "Type I" excitability (high gA). Regardless of gA, cells transform common input fluctuations into a ten- dency to spike nearly simultaneously. However, this process is more pronounced at low gA values, as previously predicted by reduced "phase" models. Thus, for a given level of common input, Type II neurons produce spikes that are relatively more correlated over short time scales. Over long time scales, the trend reverses, with Type II neurons producing relatively less correlated spike trains. This is because these cells' increased tendency for simultaneous spiking is balanced by opposing tendencies at larger time lags. We demonstrate a novel implication for neural signal processing: downstream cells with long time constants are selectively driven by Type I cell populations upstream, and those with short time constants by Type II cell populations. Our results are established via high-throughput numerical simulations, and explained via the cells' filtering properties and nonlinear dynamics.

preprint2011arXiv

The what and where of adding channel noise to the Hodgkin-Huxley equations

One of the most celebrated successes in computational biology is the Hodgkin-Huxley framework for modeling electrically active cells. This framework, expressed through a set of differential equations, synthesizes the impact of ionic currents on a cell's voltage -- and the highly nonlinear impact of that voltage back on the currents themselves -- into the rapid push and pull of the action potential. Latter studies confirmed that these cellular dynamics are orchestrated by individual ion channels, whose conformational changes regulate the conductance of each ionic current. Thus, kinetic equations familiar from physical chemistry are the natural setting for describing conductances; for small-to-moderate numbers of channels, these will predict fluctuations in conductances and stochasticity in the resulting action potentials. At first glance, the kinetic equations provide a far more complex (and higher-dimensional) description than the original Hodgkin-Huxley equations. This has prompted more than a decade of efforts to capture channel fluctuations with noise terms added to the Hodgkin-Huxley equations. Many of these approaches, while intuitively appealing, produce quantitative errors when compared to kinetic equations; others, as only very recently demonstrated, are both accurate and relatively simple. We review what works, what doesn't, and why, seeking to build a bridge to well-established results for the deterministic Hodgkin-Huxley equations. As such, we hope that this review will speed emerging studies of how channel noise modulates electrophysiological dynamics and function. We supply user-friendly Matlab simulation code of these stochastic versions of the Hodgkin-Huxley equations on the ModelDB website (accession number 138950) and http://www.amath.washington.edu/~etsb/tutorials.html.

preprint2010arXiv

On stochastic differential equation models for ion channel noise in Hodgkin-Huxley neurons

The random transitions of ion channels between conducting and non-conducting states generate a source of internal fluctuations in a neuron, known as channel noise. The standard method for modeling fluctuations in the states of ion channels uses continuous-time Markov chains nonlinearly coupled to a differential equation for voltage. Beginning with the work of Fox and Lu, there have been attempts to generate simpler models that use stochastic differential equation (SDEs) to approximate the stochastic spiking activity produced by Markov chain models. Recent numerical investigations, however, have raised doubts that SDE models can preserve the stochastic dynamics of Markov chain models. We analyze three SDE models that have been proposed as approximations to the Markov chain model: one that describes the states of the ion channels and two that describe the states of the ion channel subunits. We show that the former channel-based approach can capture the distribution of channel noise and its effect on spiking in a Hodgkin-Huxley neuron model to a degree not previously demonstrated, but the latter two subunit-based approaches cannot. Our analysis provides intuitive and mathematical explanations for why this is the case: the temporal correlation in the channel noise is determined by the combinatorics of bundling subunits into channels, and the subunit-based approaches do not correctly account for this structure. Our study therefore confirms and elucidates the findings of previous numerical investigations of subunit-based SDE models. Moreover, it presents the first evidence that Markov chain models of the nonlinear, stochastic dynamics of neural membranes can be accurately approximated by SDEs. This finding opens a door to future modeling work using SDE techniques to further illuminate the effects of ion channel fluctuations on electrically active cells.

preprint2009arXiv

Timescales of spike-train correlation for neural oscillators with common drive

We examine the effect of the phase-resetting curve (PRC) on the transfer of correlated input signals into correlated output spikes in a class of neural models receiving noisy, super-threshold stimulation. We use linear response theory to approximate the spike correlation coefficient in terms of moments of the associated exit time problem, and contrast the results for Type I vs. Type II models and across the different timescales over which spike correlations can be assessed. We find that, on long timescales, Type I oscillators transfer correlations much more efficiently than Type II oscillators. On short timescales this trend reverses, with the relative efficiency switching at a timescale that depends on the mean and standard deviation of input currents. This switch occurs over timescales that could be exploited by downstream circuits.

preprint2007arXiv

Universal properties of correlation transfer in integrate-and-fire neurons

One of the fundamental characteristics of a nonlinear system is how it transfers correlations in its inputs to correlations in its outputs. This is particularly important in the nervous system, where correlations between spiking neurons are prominent. Using linear response and asymptotic methods for pairs of unconnected integrate-and-fire (IF) neurons receiving white noise inputs, we show that this correlation transfer depends on the output spike firing rate in a strong, stereotyped manner, and is, surprisingly, almost independent of the interspike variance. For cells receiving heterogeneous inputs, we further show that correlation increases with the geometric mean spiking rate in the same stereotyped manner, greatly extending the generality of this relationship. We present an immediate consequence of this relationship for population coding via tuning curves.