Spatially-embedded, field-generating recurrent neural networks for multiscale neural computation
★ Adrián Fernández Amil
★ guarantor: Adrián Fernández Amil · vouches for the paper per WP0084 §6
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Contemporary models of neural computation are largely influenced by the neuron doctrine, treating brain function as arising from pairwise synaptic interactions at the neuronal level while neglecting macroscopic, higher-order variables generated by coordinated neural populations. This reductionist bias leaves the role of endogenous electric fields and other emergent collective dynamics insufficiently understood, preventing a closed account of cross-scale circular causation in neural systems. Evidence from multiple levels of analysis suggests that neural computation is better captured by higher-order structure than by single-unit activity. Whereas neurons exhibit substantial trial-to-trial variability, recurrent neural networks trained on cognitive tasks converge to low-dimensional population manifolds despite heterogeneous connectivity. In parallel, neural electric fields display structural invariances consistent with equivalence across microscopic configurations (i.e., multiple realizability within a degenerate design space), suggesting that higher-order variables such as population dynamics and electric fields may constitute stable computational substrates underlying robust behavior and cognition. Here, we introduce Field-Generating Recurrent Neural Networks (FG-RNNs), spatially embedded, end-to-end differentiable recurrent networks in which neural activity generates a macroscopic electric field that in turn modulates neuronal dynamics, forming a closed-loop, trainable multiscale system. We investigate the extent to which this field-mediated coupling introduces additional computational degrees of freedom that support coordinated dynamics for information encoding, transmission, and retrieval, as well as more complex functions such as compositional representation and long-horizon prediction. To this end, we train FG-RNNs on standard cognitive tasks and analyze how closing the neural-field loop induces emergent spatiotemporal structure, including traveling waves and signatures of cross-frequency coupling. Using information-theoretic and geometric analyses, we quantify when field dynamics carry task-relevant information beyond neural activity alone, providing a framework to assess whether endogenous electric fields constitute functional computational entities in their own right within the neural systems that generate them.
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