SearcharxivSearch

arXiv subjects

Christopher W. Lynn

Publications and source records attributed to Christopher W. Lynn.

At least 19 recordsLinked to original sources

Emergence of criticality in models of real neurons

Critical systems sit near boundaries between qualitatively distinct behaviors. When inferring models of neural activity, this proximity to criticality is thought to require the precise tuning of parameters. Here, we show that as the number of neurons increases, criticality can emerge naturally without fine-tuning. When computing observable statistics from parameters (the forward problem), some small regions in parameter space map to large regions in statistics space. These special parameters are precisely those near criticality. Thus, when inferring parameters from experimental measurements (the inverse problem), models concentrate near critical points, and this concentration becomes stronger as the system grows. We illustrate this flow toward criticality across many large-scale recordings in the mouse brain. In the Curie-Weiss model of Ising spins, we find that all of the recordings collapse to a first-order phase transition, despite substantial differences in the underlying systems. Together, these results suggest a resolution to the tension between criticality and fine-tuning in models of neural activity.

physics.bio-ph

Direct dependencies between neurons explain activity

Our understanding of neural computation is founded on the assumption that neurons fire in response to a linear summation of inputs. Yet experiments demonstrate that some neurons are capable of complex functions that require interactions between inputs. Here we show, across multiple brain regions and species, that direct dependencies (without interactions between inputs) explain most of the variability in neuronal activity. Neurons are quantitatively described by models that capture the measured dependence on each input individually, but assume nothing about combinations of inputs. These minimal models, which are equivalent to logistic artificial neurons, predict complex higher-order dependencies and recover known features of synaptic connectivity. The inferred neural network is sparse, indicating a highly redundant neural code that is robust to perturbations. These results suggest that, despite intricate biophysical details, most neurons are described by simple artificial models.

physics.bio-ph

Irreversible behavior drives neural flows in the hippocampus

In the brain, neural activity undergoes directed flows between states, thus breaking time-reversal symmetry. At the same time, animals also exhibit irreversible flows between behavioral states. Yet it remains unclear whether -- and how -- irreversibility in the brain relates to irreversibility in behavior. Here, we explore this connection in the hippocampus, where neural activity encodes physical location. We show that hippocampal irreversibility can be quantified using the time-delayed cross-correlations between neurons. As a mouse moves along a virtual track, we find that physical flows through the animal's environment generate neural flows through its cognitive map. Strikingly, this neural irreversibility is explained by a minimal model with only three parameters: the average velocity of the mouse, the variance in this velocity, and the resolution of the neural encoding. Together, these results provide a mechanistic understanding of irreversibility in the hippocampus and shed light on the links between symmetry breaking in the brain and behavior.

q-bio.NC

Decomposing Non-Markovian History Dependence

Non-Markovian stochastic processes are ubiquitous in biology. Nevertheless, we lack a general framework for quantifying historical dependencies. In this Letter, we propose an information-theoretic approach to decompose history dependence in systems with non-Markovian dynamics, quantifying the information encoded in dependencies of each order. In minimal models of non-Markovian dynamics, we show that this framework correctly captures the underlying historical dependencies, even when autocorrelations do not. In prolonged recordings of fly behavior, we find that the scaling of non-Markovian dependencies is invariant across timescales from fractions of a second to minutes. Despite this invariance, the overall amount of non-Markovian information is non-monotonic, suggesting a unique timescale on which historical dependencies are strongest.

cond-mat.stat-mech

Tractable Model for Tunable Non-Markovian Dynamics

Non-Markovian dynamics are ubiquitous across physics, biology, and engineering. Yet our understanding of non-Markovian processes significantly lags that of simpler Markovian processes, due largely to a lack of tractable models. In this article, we present a minimal model of non-Markovian dynamics in which the current state copies past states with arbitrary history dependence. We show that many properties of this process can be studied analytically, providing insight into the relationships between history dependence, autocorrelations, and information-theoretic metrics like entropy and dynamical information. Strikingly, we find that autocorrelations can fail, even qualitatively, to capture the underlying dependencies. Ultimately, this model serves as a tractable sandbox for exploring non-Markovian dynamics.

cond-mat.stat-mech

Quantifying the compressibility of the human brain

In the human brain, the allowed patterns of activity are constrained by the correlations between brain regions. Yet it remains unclear which correlations -- and how many -- are needed to predict large-scale neural activity. Here, we present an information-theoretic framework to identify the most important correlations, which provide the most accurate predictions of neural states. Applying our framework to cortical activity in humans, we discover that the vast majority of variance in activity is explained by a small number of correlations. This means that the brain is highly compressible: only a sparse network of correlations is needed to predict large-scale activity. We find that this compressibility is strikingly consistent across different individuals and cognitive tasks, and that, counterintuitively, the most important correlations are not necessarily the strongest. Together, these results suggest that nearly all correlations are not needed to predict neural activity, and we provide the tools to uncover the key correlations that are.

physics.bio-ph

Ising dynamics on multilayer networks with heterogeneous layers

Multilayer networks provide a framework to study complex systems with multiple types of interactions, multiple dynamical processes, and/or multiple subsystems. When studying a dynamical process on a multilayer network, it is important to consider how both layer structure and heterogeneity across layers impacts the overall dynamics. As a concrete example, we study Ising dynamics on multilayer networks and investigate how network structure affects its qualitative features. We focus primarily on multiplex networks, which are multilayer networks in which interlayer edges occur only between manifestations of the same entity on different layers, although we also consider one empirical example with a more general multilayer structure. We use numerical simulations and a mean-field approximation to examine the steady-state behavior of the Ising dynamics as a function of temperature (which is a key model parameter) for a variety of two-layer multilayer networks from both models and empirical data. We examine both the steady-state behavior and a metastable state in which the two layers are anti-aligned, and we explore the effects of interlayer coupling strength and structural heterogeneity. In synthetic multilayer networks with core--periphery structure, we show that interlayer edges that involve peripheral nodes can exert more influence than interlayer edges that involve only core nodes. Finally, we consider empirical multilayer networks from biological and social systems. Our work illustrates how heterogeneity across the layers of a multilayer network influences dynamics on the whole network.

physics.soc-ph

Neural subspaces, minimax entropy, and mean-field theory for networks of neurons

Recent advances in experimental techniques enable the simultaneous recording of activity from thousands of neurons in the brain, presenting both an opportunity and a challenge: to build meaningful, scalable models of large neural populations. Correlations in the brain are typically weak but widespread, suggesting that a mean-field approach might be effective in describing real neural populations, and we explore a hierarchy of maximum entropy models guided by this idea. We begin with models that match only the mean and variance of the total population activity, and extend to models that match the experimentally observed mean and variance of activity along multiple projections of the neural state. Confronted by data from several different brain regions, these models are driven toward a first-order phase transition, characterized by the presence of two nearly degenerate minima in the energy landscape, and this leads to predictions in qualitative disagreement with other features of the data. To resolve this problem we introduce a novel class of models that constrain the full probability distribution of activity along selected projections. We develop the mean-field theory for this class of models and apply it to recordings from 1000+ neurons in the mouse hippocampus. This 'distributional mean--field' model provides an accurate and consistent description of the data, offering a scalable and principled approach to modeling complex neural population dynamics.

physics.bio-ph

Coarse-graining dynamics to maximize irreversibility

In many far-from-equilibrium biological systems, energy injected by irreversible processes at microscopic scales propagates to larger scales to fulfill important biological functions. But given dissipative dynamics at the microscale, how much irreversibility can persist at the macroscale? Here, we propose a model-free coarse-graining procedure that merges microscopic states to minimize the amount of lost irreversibility. Beginning with dynamical measurements, this procedure produces coarse-grained dynamics that retain as much information as possible about the underlying irreversibility. In synthetic and experimental data spanning molecular motors, biochemical oscillators, and recordings of neural activity, we derive simplified descriptions that capture the essential nonequilibrium processes. These results provide the tools to study the fundamental limits on the emergence of macroscopic irreversibility.

cond-mat.stat-mech

Minimax entropy: The statistical physics of optimal models

When constructing models of the world, we aim for optimal compressions: models that include as few details as possible while remaining as accurate as possible. But which details -- or features measured in data -- should we choose to include in a model? Here, using the minimum description length principle, we show that the optimal features are the ones that produce the maximum entropy model with minimum entropy, thus yielding a minimax entropy principle. We review applications, which range from machine learning to optimal models of biological networks. Naive implementations, however, are limited to systems with small numbers of states and features. We therefore require new theoretical insights and computational techniques to construct optimal compressions of high-dimensional datasets arising in large-scale experiments.

q-bio.QM

Extended mean-field theories for networks of real neurons

If the behavior of a system with many degrees of freedom can be captured by a small number of collective variables, then plausibly there is an underlying mean-field theory. We show that simple versions of this idea fail to describe the patterns of activity in networks of real neurons. An extended mean-field theory that matches the distribution of collective variables is at least consistent, though shows signs that these networks are poised near a critical point, in agreement with other observations. These results suggest a path to analysis of emerging data on ever larger numbers of neurons.

physics.bio-ph

Statistical physics of large-scale neural activity with loops

As experiments advance to record from tens of thousands of neurons, statistical physics provides a framework for understanding how collective activity emerges from networks of fine-scale correlations. While modeling these populations is tractable in loop-free networks, neural circuitry inherently contains feedback loops of connectivity. Here, for a class of networks with loops, we present an exact solution to the maximum entropy problem that scales to very large systems. This solution provides direct access to information-theoretic measures like the entropy of the model and the information contained in correlations, which are usually inaccessible at large scales. In turn, this allows us to search for the optimal network of correlations that contains the maximum information about population activity. Applying these methods to 45 recordings of approximately 10,000 neurons in the mouse visual system, we demonstrate that our framework captures more information -- providing a better description of the population -- than existing methods without loops. For a given population, our models perform even better during visual stimulation than spontaneous activity; however, the inferred interactions overlap significantly, suggesting an underlying neural circuitry that remains consistent across stimuli. Generally, we construct an optimized framework for studying the statistical physics of large neural populations, with future applications extending to other biological networks.

physics.bio-ph

Exact minimax entropy models of large-scale neuronal activity

In the brain, fine-scale correlations combine to produce macroscopic patterns of activity. However, as experiments record from larger and larger populations, we approach a fundamental bottleneck: the number of correlations one would like to include in a model grows larger than the available data. In this undersampled regime, one must focus on a sparse subset of correlations; the optimal choice contains the maximum information about patterns of activity or, equivalently, minimizes the entropy of the inferred maximum entropy model. Applying this ``minimax entropy" principle is generally intractable, but here we present an exact and scalable solution for pairwise correlations that combine to form a tree (a network without loops). Applying our method to over one thousand neurons in the mouse hippocampus, we find that the optimal tree of correlations reduces our uncertainty about the population activity by 14% (over 50 times more than a random tree). Despite containing only 0.1% of all pairwise correlations, this minimax entropy model accurately predicts the observed large-scale synchrony in neural activity and becomes even more accurate as the population grows. The inferred Ising model is almost entirely ferromagnetic (with positive interactions) and exhibits signatures of thermodynamic criticality. These results suggest that a sparse backbone of excitatory interactions may play an important role in driving collective neuronal activity.

physics.bio-ph

Exactly solvable statistical physics models for large neuronal populations

Maximum entropy methods provide a principled path connecting measurements of neural activity directly to statistical physics models, and this approach has been successful for populations of $N\sim 100$ neurons. As $N$ increases in new experiments, we enter an undersampled regime where we have to choose which observables should be constrained in the maximum entropy construction. The best choice is the one that provides the greatest reduction in entropy, defining a "minimax entropy" principle. This principle becomes tractable if we restrict attention to correlations among pairs of neurons that link together into a tree; we can find the best tree efficiently, and the underlying statistical physics models are exactly solved. We use this approach to analyze experiments on $N\sim 1500$ neurons in the mouse hippocampus, and show that the resulting model captures the distribution of synchronous activity in the network.

physics.bio-ph

Spontaneous brain activity emerges from pairwise interactions in the larval zebrafish brain

Brain activity is characterized by brain-wide spatiotemporal patterns which emerge from synapse-mediated interactions between individual neurons. Calcium imaging provides access to in vivo recordings of whole-brain activity at single-neuron resolution and, therefore, allows the study of how large-scale brain dynamics emerge from local activity. In this study, we used a statistical mechanics approach - the pairwise maximum entropy model (MEM) - to infer microscopic network features from collective patterns of activity in the larval zebrafish brain, and relate these features to the emergence of observed whole-brain dynamics. Our findings indicate that the pairwise interactions between neural populations and their intrinsic activity states are sufficient to explain observed whole-brain dynamics. In fact, the pairwise relationships between neuronal populations estimated with the MEM strongly correspond to observed structural connectivity patterns. Model simulations also demonstrated how tuning pairwise neuronal interactions drives transitions between critical and pathologically hyper-excitable whole-brain regimes. Finally, we use virtual resection to identify the brain structures that are important for maintaining the brain in a critical regime. Together, our results indicate that whole-brain activity emerges out of a complex dynamical system that transitions between basins of attraction whose strength and topology depend on the connectivity between brain areas.

q-bio.NC

Human Learning of Hierarchical Graphs

Humans are constantly exposed to sequences of events in the environment. Those sequences frequently evince statistical regularities, such as the probabilities with which one event transitions to another. Collectively, inter-event transition probabilities can be modeled as a graph or network. Many real-world networks are organized hierarchically and understanding how humans learn these networks is an ongoing aim of current investigations. While much is known about how humans learn basic transition graph topology, whether and to what degree humans can learn hierarchical structures in such graphs remains unknown. We investigate how humans learn hierarchical graphs of the Sierpiński family using computer simulations and behavioral laboratory experiments. We probe the mental estimates of transition probabilities via the surprisal effect: a phenomenon in which humans react more slowly to less expected transitions, such as those between communities or modules in the network. Using mean-field predictions and numerical simulations, we show that surprisal effects are stronger for finer-level than coarser-level hierarchical transitions. Surprisal effects at coarser levels of the hierarchy are difficult to detect for limited learning times or in small samples. Using a serial response experiment with human participants (n=$100$), we replicate our predictions by detecting a surprisal effect at the finer-level of the hierarchy but not at the coarser-level of the hierarchy. To further explain our findings, we evaluate the presence of a trade-off in learning, whereby humans who learned the finer-level of the hierarchy better tended to learn the coarser-level worse, and vice versa. Our study elucidates the processes by which humans learn hierarchical sequential events. Our work charts a road map for future investigation of the neural underpinnings and behavioral manifestations of graph learning.

q-bio.NC

Information content of note transitions in the music of J. S. Bach

Music has a complex structure that expresses emotion and conveys information. Humans process that information through imperfect cognitive instruments that produce a gestalt, smeared version of reality. How can we quantify the information contained in a piece of music? Further, what is the information inferred by a human, and how does that relate to (and differ from) the true structure of a piece? To tackle these questions quantitatively, we present a framework to study the information conveyed in a musical piece by constructing and analyzing networks formed by notes (nodes) and their transitions (edges). Using this framework, we analyze music composed by J. S. Bach through the lens of network science and information theory. Regarded as one of the greatest composers in the Western music tradition, Bach's work is highly mathematically structured and spans a wide range of compositional forms, such as fugues and choral pieces. Conceptualizing each composition as a network of note transitions, we quantify the information contained in each piece and find that different kinds of compositions can be grouped together according to their information content and network structure. Moreover, we find that the music networks communicate large amounts of information while maintaining small deviations of the inferred network from the true network, suggesting that they are structured for efficient communication of information. We probe the network structures that enable this rapid and efficient communication of information--namely, high heterogeneity and strong clustering. Taken together, our findings shed new light on the information and network properties of Bach's compositions. More generally, our framework serves as a stepping stone for exploring musical complexities, creativity and the structure of information in a range of complex systems.

physics.soc-ph

Emergent scale-free networks

Many complex systems--from social and communication networks to biological networks and the Internet--are thought to exhibit scale-free structure. However, prevailing explanations rely on the constant addition of new nodes, an assumption that fails dramatically in some real-world settings. Here, we propose a model in which nodes are allowed to die, and their connections rearrange under a mixture of preferential and random attachment. With these simple dynamics, we show that networks self-organize towards scale-free structure, with a power-law exponent $γ= 1 + \frac{1}{p}$ that depends only on the proportion $p$ of preferential (rather than random) attachment. Applying our model to several real networks, we infer $p$ directly from data, and predict the relationship between network size and degree heterogeneity. Together, these results establish that realistic scale-free structure can emerge naturally in networks of constant size and density, with broad implications for the structure and function of complex systems.

nlin.AO