Biology subjects

Zavatone-Veth, J. A.

Publications and source records attributed to Zavatone-Veth, J. A..

10 recordsLinked to original sources

bioRxiv2026

Structure, disorder, and dynamics in task-trained recurrent neural circuits

Across many brain areas, neurons produce heterogeneous, seemingly disordered responses. Yet such circuits cannot be purely random, since they must possess some structure to generate the representations and computations underlying behavior. How much structure is present in recurrent connectivity relative to disorder, and how the interaction between the two shapes population dynamics and single-neuron responses, remain incompletely understood. Recurrent neural networks trained to perform tasks have become a leading model of such circuits, but conventional training yields a single point in a vast space of task-compatible solutions, with no systematic way to explore this space and no theory of how internal representations vary within it. Without such a theory, the questions above cannot be addressed, and comparisons between trained networks and neural data are difficult to interpret. Here, we introduce a control parameter that governs the degree to which learning reshapes recurrent connectivity, interpolating between a reservoir regime and one in which recurrent weights are restructured by learning to produce task-relevant internal representations. Varying this parameter generates a family of task-compatible solutions whose internal dynamics differ in a controlled and interpretable way. We derive a dynamical mean-field theory showing that, while population-level dynamics converge to a deterministic limit, individual neurons are driven by independent samples from a single-neuron input-current distribution. When connectivity is random, this distribution is Gaussian. Recurrent restructuring drives it toward task-dependent, non-Gaussian forms. In linear networks, restructuring amplifies task-relevant frequencies. In nonlinear networks, it drives a phase transition from chaotic, high-dimensional activity to ordered, low-dimensional dynamics that generalize temporally beyond the training period. We apply the theory to a reaching task in which a recurrent network must reproduce macaque muscle activity, and find that optimally matching simultaneous motor-cortex recordings requires only a small degree of restructuring, with learned structure coexisting with random heterogeneity. These results suggest a broader picture in which large recurrent circuits are largely random but contain, to varying degrees, structured recurrent connectivity sufficient for generalizable, task-relevant representations.1

neuroscience↗

bioRxiv2025

Simultaneous detection and estimation in olfactory sensing

The mammalian olfactory system shows an exceptional ability for rapid and accurate decoding of both the identity and concentration of odorants. Previous works have used the theory of compressed sensing to elucidate the algorithmic basis for this capability: decoding odor information from the responses of a restricted repertoire of receptors is possible because only a few relevant odorants are present in any given sensory scene. However, existing circuit models for olfactory decoding still cannot contend with the complexity of naturalistic olfactory scenes; they are limited to detection of a handful of odorants. Here, we propose a model for olfactory compressed sensing inspired by simultaneous localization and mapping algorithms in navigation, in which the set of present odors and their concentrations are inferred separately. We implement this split inference in a biologically-plausible recurrent circuit by introducing separate dynamics matched to the distinct nature of presence and concentration, and drawing on the framework of Mirrored Langevin Dynamics. This model can accurately infer presence and concentration at scale. Moreover, its circuit structure can be mapped onto the primary cell types of the olfactory bulb, giving a possible normative account for functional differences between mitral and tufted cells. Our approach offers a general path towards circuit algorithms for probabilistic inference--in olfactory sensing and beyond--that both perform well in naturalistic environments and make experimentally-testable predictions for neural response dynamics.

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bioRxiv2025

Convergent motifs of early olfactory processing are recapitulated by layer-wise efficient coding

The architecture of early olfactory processing is a striking example of convergent evolution. Typically, a panel of broadly tuned receptors is selectively expressed in sensory neurons (each neuron expressing only one receptor), and each glomerulus receives projections from just one neuron type. Taken together, these three motifs--broad receptors, selective expression, and glomerular convergence--constitute "canonical olfaction," since a number of model organisms including mice and flies exhibit these features. The emergence of this distinctive architecture across evolutionary lineages suggests that it may be optimized for information processing, an idea known as efficient coding. In this work, we show that by maximizing mutual information one layer at a time, efficient coding recovers several features of canonical olfactory processing under realistic biophysical assumptions. We also explore the settings in which noncanonical olfaction may be advantageous. Along the way, we make several predictions relating olfactory circuits to features of receptor families and the olfactory environment.

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bioRxiv2025

Combining Sampling Methods with Attractor Dynamics in Spiking Models of Head-Direction Systems

Uncertainty is a fundamental aspect of the natural environment, requiring the brain to infer and integrate noisy signals to guide behavior effectively. Sampling-based inference has been proposed as a mechanism for dealing with uncertainty, particularly in early sensory processing. However, it is unclear how to reconcile sampling-based methods with operational principles of higher-order brain areas, such as attractor dynamics of persistent neural representations. In this study, we present a spiking neural network model for the head-direction (HD) system that combines sampling-based inference with attractor dynamics. To achieve this, we derive the required spiking neural network dynamics and interactions to perform sampling from a large family of probability distributions--including variables encoded with Poisson noise. We then propose a method that allows the network to update its estimate of the current head direction by integrating angular velocity samples--derived from noisy inputs--with a pull towards a circular manifold, thereby maintaining consistent attractor dynamics. This model makes specific, testable predictions about the HD system that can be examined in future neurophysiological experiments: it predicts correlated subthreshold voltage fluctuations; distinctive short- and long-term firing correlations among neurons; and characteristic statistics of the movement of the neural activity "bump" representing the head direction. Overall, our approach extends previous theories on probabilistic sampling with spiking neurons, offers a novel perspective on the computations responsible for orientation and navigation, and supports the hypothesis that sampling-based methods can be combined with attractor dynamics to provide a viable framework for studying neural dynamics across the brain.

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bioRxiv2024

A Model of Place Field Reorganization During Reward Maximization

When rodents learn to navigate in a novel environment, a high density of place fields emerges at reward locations, fields elongate against the trajectory, and individual fields change spatial selectivity while demonstrating stable behavior. Why place fields demonstrate these characteristic phenomena during learning remains elusive. We develop a normative framework using a reward maximization objective, whereby the temporal difference (TD) error drives place field reorganization to improve policy learning. Place fields are modeled using Gaussian radial basis functions to represent states in an environment, and directly synapse to an actor-critic for policy learning. Each field's amplitude, center, and width, as well as downstream weights, are updated online at each time step to maximize cumulative reward. We demonstrate that this framework unifies three disparate phenomena observed in navigation experiments. Furthermore, we show that these place field phenomena improve policy convergence when learning to navigate to a single target and relearning multiple new targets. To conclude, we develop a normative model that recapitulates several aspects of hippocampal place field learning dynamics and unifies mechanisms to offer testable predictions for future experiments.

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bioRxiv2024

Partial observation can induce mechanistic mismatches in data-constrained models of neural dynamics

One of the central goals of neuroscience is to gain a mechanistic understanding of how the dynamics of neural circuits give rise to their observed function. A popular approach towards this end is to train recurrent neural networks (RNNs) to reproduce experimental recordings of neural activity. These trained RNNs are then treated as surrogate models of biological neural circuits, whose properties can be dissected via dynamical systems analysis. How reliable are the mechanistic insights derived from this procedure? While recent advances in population-level recording technologies have allowed simultaneous recording of up to tens of thousands of neurons, this represents only a tiny fraction of most cortical circuits. Here we show that observing only a subset of neurons in a circuit can create mechanistic mismatches between a simulated teacher network and a data-constrained student, even when the two networks have matching single-unit dynamics. In particular, partial observation of models of low-dimensional cortical dynamics based on functionally feedforward or low-rank connectivity can lead to surrogate models with spurious attractor structure. Our results illustrate the challenges inherent in accurately uncovering neural mechanisms from single-trial data, and suggest the need for new methods of validating data-constrained models for neural dynamics.

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bioRxiv2023

Neural circuits for fast Poisson compressed sensing in the olfactory bulb

Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result, the olfactory system must solve a compressed sensing problem, relying on the fact that only a handful of the millions of possible odorants are present in a given scene. Inspired by this principle, past works have proposed normative compressed sensing models for olfactory decoding. However, these models have not captured the unique anatomy and physiology of the olfactory bulb, nor have they shown that sensing can be achieved within the 100-millisecond timescale of a single sniff. Here, we propose a rate-based Poisson compressed sensing circuit model for the olfactory bulb. This model maps onto the neuron classes of the olfactory bulb, and recapitulates salient features of their connectivity and physiology. For circuit sizes comparable to the human olfactory bulb, we show that this model can accurately detect tens of odors within the timescale of a single sniff. We also show that this model can perform Bayesian posterior sampling for accurate uncertainty estimation. Fast inference is possible only if the geometry of the neural code is chosen to match receptor properties, yielding a distributed neural code that is not axis-aligned to individual odor identities. Our results illustrate how normative modeling can help us map function onto specific neural circuits to generate new hypotheses.

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bioRxiv2022

Population geometry enables fast sampling in spiking neural networks

For animals to navigate an uncertain world, their brains need to estimate uncertainty at the timescales of sensations and actions. Sampling-based algorithms afford a theoretically-grounded framework for probabilistic inference in neural circuits, but it remains unknown how one can implement fast sampling algorithms in biologically-plausible spiking networks. Here, we propose to leverage the population geometry, controlled by the neural code and the neural dynamics, to implement fast samplers in spiking neural networks. We first show that two classes of spiking samplers--efficient balanced spiking networks that simulate Langevin sampling, and networks with probabilistic spike rules that implement Metropolis-Hastings sampling--can be unified within a common framework. We then show that careful choice of population geometry, corresponding to the natural space of parameters, enables rapid inference of parameters drawn from strongly-correlated high-dimensional distributions in both networks. Our results suggest design prin-ciples for algorithms for sampling-based probabilistic inference in spiking neural networks, yielding potential inspiration for neuromorphic computing and testable predictions for neurobiology.

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bioRxiv2021

Manipulating neural dynamics to tune motion detection

Neurons integrate excitatory and inhibitory signals to produce their outputs, but the role of input timing in this integration remains poorly understood. Motion detection is a paradigmatic example of this integration, since theories of motion detection rely on different delays in visual signals. These delays allow circuits to compare scenes at different times to calculate the direction and speed of motion. It remains untested how response dynamics of individual cell types drive motion detection and velocity sensitivity. Here, we sped up or slowed down specific neuron types in Drosophilas motion detection circuit by manipulating ion channel expression. Altering the dynamics of individual neurons upstream of motion detectors changed their integrating properties and increased their sensitivity to fast or slow visual motion, exposing distinct roles for dynamics in tuning directional signals. A circuit model constrained by data and anatomy reproduced the observed tuning changes. Together, these results reveal how excitatory and inhibitory dynamics jointly tune a canonical circuit computation.

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bioRxiv2020

Statistical structure of the trial-to-trial timing variability in synfire chains

Timing and its variability are crucial for behavior. Consequently, neural circuits that take part in the control of timing and in the measurement of temporal intervals have been the subject of much research. Here, we provide an analytical and computational account of the temporal variability in what is perhaps the most basic model of a timing circuit, the synfire chain. First, we study the statistical structure of trial-to-trial timing variability in a reduced but analytically tractable model: a chain of single integrate-and-fire neurons. We show that this circuits variability is well-described by a generative model consisting of local, global, and jitter components. We relate each of these components to distinct neural mechanisms in the model. Next, we establish in simulations that these results carry over to a noisy homogeneous synfire chain. Finally, motivated by the fact that a synfire chain is thought to underlie the circuit that takes part in the control and timing of zebra finch song, we present simulations of a biologically realistic synfire chain model of the zebra finch timekeeping circuit. We find the structure of trial-to-trial timing variability to be consistent with our previous findings, and to agree with experimental observations of the songs temporal variability. Our study therefore provides a possible neuronal account of behavioral variability in zebra finches.

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