Probing neural population dynamics with recurrent neural networks
Large-scale recordings of neural activity are providing new opportunities to study network-level dynamics with unprecedented detail. However, the sheer volume of data and its dynamical complexity are major barriers to uncovering and interpreting these dynamics. I will present latent factor analysis via dynamical systems, a sequential autoencoding approach that enables inference of dynamics from neuronal population spiking activity on single trials and millisecond timescales. I will also discuss recent adaptations of the method to uncover dynamics from neural activity recorded via 2P Calcium imaging. Finally, time permitting, I will mention recent efforts to improve the interpretability of deep-learning based dynamical systems models.
Reimagining the neuron as a controller: A novel model for Neuroscience and AI
We build upon and expand the efficient coding and predictive information models of neurons, presenting a novel perspective that neurons not only predict but also actively influence their future inputs through their outputs. We introduce the concept of neurons as feedback controllers of their environments, a role traditionally considered computationally demanding, particularly when the dynamical system characterizing the environment is unknown. By harnessing a novel data-driven control framework, we illustrate the feasibility of biological neurons functioning as effective feedback controllers. This innovative approach enables us to coherently explain various experimental findings that previously seemed unrelated. Our research has profound implications, potentially revolutionizing the modeling of neuronal circuits and paving the way for the creation of alternative, biologically inspired artificial neural networks.
The balance hypothesis for the avian lumbosacral organ and an exploration of its morphological variation
The centrality of population-level factors to network computation is demonstrated by a versatile approach for training spiking networks
Neural activity is often described in terms of population-level factors extracted from the responses of many neurons. Factors provide a lower-dimensional description with the aim of shedding light on network computations. Yet, mechanistically, computations are performed not by continuously valued factors but by interactions among neurons that spike discretely and variably. Models provide a means of bridging these levels of description. We developed a general method for training model networks of spiking neurons by leveraging factors extracted from either data or firing-rate-based networks. In addition to providing a useful model-building framework, this formalism illustrates how reliable and continuously valued factors can arise from seemingly stochastic spiking. Our framework establishes procedures for embedding this property in network models with different levels of realism. The relationship between spikes and factors in such networks provides a foundation for interpreting (and subtly redefining) commonly used quantities such as firing rates.
Extracting computational mechanisms from neural data using low-rank RNNs
An influential theory in systems neuroscience suggests that brain function can be understood through low-dimensional dynamics [Vyas et al 2020]. However, a challenge in this framework is that a single computational task may involve a range of dynamic processes. To understand which processes are at play in the brain, it is important to use data on neural activity to constrain models. In this study, we present a method for extracting low-dimensional dynamics from data using low-rank recurrent neural networks (lrRNNs), a highly expressive and understandable type of model [Mastrogiuseppe & Ostojic 2018, Dubreuil, Valente et al. 2022]. We first test our approach using synthetic data created from full-rank RNNs that have been trained on various brain tasks. We find that lrRNNs fitted to neural activity allow us to identify the collective computational processes and make new predictions for inactivations in the original RNNs. We then apply our method to data recorded from the prefrontal cortex of primates during a context-dependent decision-making task. Our approach enables us to assign computational roles to the different latent variables and provides a mechanistic model of the recorded dynamics, which can be used to perform in silico experiments like inactivations and provide testable predictions.
Neural Population Dynamics for Skilled Motor Control
The ability to reach, grasp, and manipulate objects is a remarkable expression of motor skill, and the loss of this ability in injury, stroke, or disease can be devastating. These behaviors are controlled by the coordinated activity of tens of millions of neurons distributed across many CNS regions, including the primary motor cortex. While many studies have characterized the activity of single cortical neurons during reaching, the principles governing the dynamics of large, distributed neural populations remain largely unknown. Recent work in primates has suggested that during the execution of reaching, motor cortex may autonomously generate the neural pattern controlling the movement, much like the spinal central pattern generator for locomotion. In this seminar, I will describe recent work that tests this hypothesis using large-scale neural recording, high-resolution behavioral measurements, dynamical systems approaches to data analysis, and optogenetic perturbations in mice. We find, by contrast, that motor cortex requires strong, continuous, and time-varying thalamic input to generate the neural pattern driving reaching. In a second line of work, we demonstrate that the cortico-cerebellar loop is not critical for driving the arm towards the target, but instead fine-tunes movement parameters to enable precise and accurate behavior. Finally, I will describe my future plans to apply these experimental and analytical approaches to the adaptive control of locomotion in complex environments.
Credit Assignment in Neural Networks through Deep Feedback Control
The success of deep learning sparked interest in whether the brain learns by using similar techniques for assigning credit to each synaptic weight for its contribution to the network output. However, the majority of current attempts at biologically-plausible learning methods are either non-local in time, require highly specific connectivity motives, or have no clear link to any known mathematical optimization method. Here, we introduce Deep Feedback Control (DFC), a new learning method that uses a feedback controller to drive a deep neural network to match a desired output target and whose control signal can be used for credit assignment. The resulting learning rule is fully local in space and time and approximates Gauss-Newton optimization for a wide range of feedback connectivity patterns. To further underline its biological plausibility, we relate DFC to a multi-compartment model of cortical pyramidal neurons with a local voltage-dependent synaptic plasticity rule, consistent with recent theories of dendritic processing. By combining dynamical system theory with mathematical optimization theory, we provide a strong theoretical foundation for DFC that we corroborate with detailed results on toy experiments and standard computer-vision benchmarks.
Dynamical Neuromorphic Systems
In this talk, I aim to show that the dynamical properties of emerging nanodevices can accelerate the development of smart, and environmentally friendly chips that inherently learn through their physics. The goal of neuromorphic computing is to draw inspiration from the architecture of the brain to build low-power circuits for artificial intelligence. I will first give a brief overview of the state of the art of neuromorphic computing, highlighting the opportunities offered by emerging nanodevices in this field, and the associated challenges. I will then show that the intrinsic dynamical properties of these nanodevices can be exploited at the device and algorithmic level to assemble systems that infer and learn though their physics. I will illustrate these possibilities with examples from our work on spintronic neural networks that communicate and compute through their microwave oscillations, and on an algorithm called Equilibrium Propagation that minimizes both the error and energy of a dynamical system.
Stability-Flexibility Dilemma in Cognitive Control: A Dynamical System Perspective
Constraints on control-dependent processing have become a fundamental concept in general theories of cognition that explain human behavior in terms of rational adaptations to these constraints. However, theories miss a rationale for why such constraints would exist in the first place. Recent work suggests that constraints on the allocation of control facilitate flexible task switching at the expense of the stability needed to support goal-directed behavior in face of distraction. We formulate this problem in a dynamical system, in which control signals are represented as attractors and in which constraints on control allocation limit the depth of these attractors. We derive formal expressions of the stability-flexibility tradeoff, showing that constraints on control allocation improve cognitive flexibility but impair cognitive stability. We provide evidence that human participants adapt higher constraints on the allocation of control as the demand for flexibility increases but that participants deviate from optimal constraints. In continuing work, we are investigating how collaborative performance of a group of individuals can benefit from individual differences defined in terms of balance between cognitive stability and flexibility.
Theory, reimagined
Physics offers countless examples for which theoretical predictions are astonishingly powerful. But it’s hard to imagine a similar precision in complex systems where the number and interdependencies between components simply prohibits a first-principles approach, look no further than the challenge of the billions of neurons and trillions of connections within our own brains. In such settings how do we even identify the important theoretical questions? We describe a systems-scale perspective in which we integrate information theory, dynamical systems and statistical physics to extract understanding directly from measurements. We demonstrate our approach with a reconstructed state space of the behavior of the nematode C. elegans, revealing a chaotic attractor with symmetric Lyapunov spectrum and a novel perspective of motor control. We then outline a maximally predictive coarse-graining in which nonlinear dynamics are subsumed into a linear, ensemble evolution to obtain a simple yet accurate model on multiple scales. With this coarse-graining we identify long timescales and collective states in the Langevin dynamics of a double-well potential, the Lorenz system and in worm behavior. We suggest that such an ``inverse’’ approach offers an emergent, quantitative framework in which to seek rather than impose effective organizing principles of complex systems.
Simons-Emory Workshop on Neural Dynamics: What could neural dynamics have to say about neural computation, and do we know how to listen?
Speakers will deliver focused 10-minute talks, with periods reserved for broader discussion on topics at the intersection of neural dynamics and computation. Organizer & Moderator: Chethan Pandarinath - Emory University and Georgia Tech Speakers & Discussants: Adrienne Fairhall - U Washington Mehrdad Jazayeri - MIT John Krakauer - John Hopkins Francesca Mastrogiuseppe - Gatsby / UCL Abigail Person - U Colorado Abigail Russo - Princeton Krishna Shenoy - Stanford Saurabh Vyas - Columbia
Pancreatic α and β cells are globally phase-locked
The Ca2+ modulated pulsatile secretions of glucagon and insulin by pancreatic α and β cells play a key role in glucose metabolism and homeostasis. However, how different types of cells in the islet couple and coordinate to give rise to various Ca2+ oscillation patterns and how these patterns are being tuned by paracrine regulation are still elusive. Here we developed a microfluidic device to facilitate long-term recording of islet Ca2+ activity at single cell level and found that islets show heterogeneous but intrinsic oscillation patterns. The α and β cells in an islet oscillate in antiphase and are globally phase locked to display a variety of oscillation modes. A mathematical model of islet oscillation maps out the dependence of the oscillation modes on the paracrine interactions between α and β cells. Our study reveals the origin of the islet oscillation patterns and highlights the role of paracrine regulation in tuning them.
Neural manifolds for the stable control of movement
Animals perform learned actions with remarkable consistency for years after acquiring a skill. What is the neural correlate of this stability? We explore this question from the perspective of neural populations. Recent work suggests that the building blocks of neural function may be the activation of population-wide activity patterns: neural modes that capture the dominant co-variation patterns of population activity and define a task specific low dimensional neural manifold. The time-dependent activation of the neural modes results in latent dynamics. We hypothesize that the latent dynamics associated with the consistent execution of a behaviour need to remain stable, and use an alignment method to establish this stability. Once identified, stable latent dynamics allow for the prediction of various behavioural features via fixed decoder models. We conclude that latent cortical dynamics within the task manifold are the fundamental and stable building blocks underlying consistent behaviour.