Interpreting and comparing neural activity across systems by geometric deep learning
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Neural circuits distributed across different brain regions mediate how neural information is processed and integrated, resulting in complex cognitive capabilities and behaviour. To understand dynamics and interactions of neural circuits, it is crucial to capture the complete spectrum of neural activity, ranging from the fast action potentials of individual neurons to the population dynamics driven by slow brain-wide oscillations. In this Review, we discuss how advances in electrical and optical recording technologies, coupled with the emergence of machine learning methodologies, present a unique opportunity to unravel the complex dynamics of the brain. Although great progress has been made in both electrical and optical neural recording technologies, these alone fail to provide a comprehensive picture of the neuronal activity with high spatiotemporal resolution. To address this challenge, multimodal experiments integrating the complementary advantages of different techniques hold great promise. However, they are still hindered by the absence of multimodal data analysis methods capable of providing unified and interpretable explanations of the complex neural dynamics distinctly encoded in these modalities. Combining multimodal studies with advanced data analysis methods will offer novel perspectives to address unresolved questions in basic neuroscience and to develop treatments for various neurological disorders.
Predictive learning as the basis of the testing effect
A prominent learning phenomenon is the testing effect, meaning that testing enhances retention more than studying. Emergent frameworks propose fundamental (Hebbian and predictive) learning principles as its basis. Predictive learning posits that learning occurs based on the contrast (error) between a prediction and the feedback on that prediction (prediction error). Here, we propose that in testing (but not studying) scenarios, participants predict potential answers, and its contrast with the subsequent feedback yields a prediction error, which facilitates testing-based learning. To investigate this, we developed an associative memory network incorporating Hebbian and/or predictive learning, together with an experimental design where human participants studied or tested English-Swahili word pairs followed by recognition. Three behavioral experiments (N = 80, 81, 62) showed robust testing effects when feedback was provided. Model fitting (of 10 different models) suggested that only models incorporating predictive learning can account for the breadth of data associated with the testing effect. Our data and model suggest that predictive learning underlies the testing effect.
MARBLE: interpretable representations of neural population dynamics using geometric deep learning
The dynamics of neuron populations commonly evolve on low-dimensional manifolds. Thus, we need methods that learn the dynamical processes over neural manifolds to infer interpretable and consistent latent representations. We introduce a representation learning method, MARBLE, which decomposes on-manifold dynamics into local flow fields and maps them into a common latent space using unsupervised geometric deep learning. In simulated nonlinear dynamical systems, recurrent neural networks and experimental single-neuron recordings from primates and rodents, we discover emergent low-dimensional latent representations that parametrize high-dimensional neural dynamics during gain modulation, decision-making and changes in the internal state. These representations are consistent across neural networks and animals, enabling the robust comparison of cognitive computations. Extensive benchmarking demonstrates state-of-the-art within- and across-animal decoding accuracy of MARBLE compared to current representation learning approaches, with minimal user input. Our results suggest that a manifold structure provides a powerful inductive bias to develop decoding algorithms and assimilate data across experiments.
Understanding learning through uncertainty and bias
Learning allows humans and other animals to make predictions about the environment that facilitate adaptive behavior. Casting learning as predictive inference can shed light on normative cognitive mechanisms that improve predictions under uncertainty. Drawing on normative learning models, we illustrate how learning should be adjusted to different sources of uncertainty, including perceptual uncertainty, risk, and uncertainty due to environmental changes. Such models explain many hallmarks of human learning in terms of specific statistical considerations that come into play when updating predictions under uncertainty. However, humans also display systematic learning biases that deviate from normative models, as studied in computational psychiatry. Some biases can be explained as normative inference conditioned on inaccurate prior assumptions about the environment, while others reflect approximations to Bayesian inference aimed at reducing cognitive demands. These biases offer insights into cognitive mechanisms underlying learning and how they might go awry in psychiatric illness.
An integrative data-driven model simulating C. elegans brain, body and environment interactions
The behavior of an organism is influenced by the complex interplay between its brain, body and environment. Existing data-driven models focus on either the brain or the body–environment. Here we present BAAIWorm, an integrative data-driven model of Caenorhabditis elegans, which consists of two submodels: the brain model and the body–environment model. The brain model was built by multicompartment models with realistic morphology, connectome and neural population dynamics based on experimental data. Simultaneously, the body–environment model used a lifelike body and a three-dimensional physical environment. Through the closed-loop interaction between the two submodels, BAAIWorm reproduced the realistic zigzag movement toward attractors observed in C. elegans. Leveraging this model, we investigated the impact of neural system structure on both neural activities and behaviors. Consequently, BAAIWorm can enhance our understanding of how the brain controls the body to interact with its surrounding environment.
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