From bioelectric fields to neural manifolds: a dynamical theory of brain development
★ Adrián Fernández Amil
★ guarantor: Adrián Fernández Amil · vouches for the paper per WP0084 §6
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Brain development is traditionally viewed as the execution of genetically specified programs that explicitly encode low-level anatomical features such as precise synaptic wiring. However, this perspective becomes difficult to reconcile with the massive combinatorial complexity of neural circuits relative to the limited information capacity of the genome. Moreover, similar computations can emerge from multiple distinct microcircuit implementations, suggesting that development may specify higher-order dynamical constraints rather than exact connectivity patterns. Here, we argue that developmental programs leverage macro-scale physiological and bioelectric gradients to sculpt circuit connectivity motifs that converge toward specific low-dimensional activity geometries. These geometries correspond to macroscopic electric field patterns that support the population dynamics underlying regional computation. In this framework, development is seen as a hierarchical process in which genes encode high-level target dynamics, while lower-level self-organizing mechanisms -- including neuronal competition, cooperation, and activity-dependent plasticity -- construct the specific microcircuits capable of realizing them. Crucially, this process exploits the gauge invariance of electric fields, allowing functional dynamics to remain stable across diverse microscopic implementations. This perspective is supported by evidence from developmental biophysics and morphogenesis, where bioelectric signaling plays a causal role in shaping organismal form. In particular, experimental manipulations of bioelectric states have been shown to steer development toward specific target morphologies in organisms such as planarian flatworms, demonstrating that large-scale physiological fields can encode instructive developmental information independently of the existing, detailed local structure. Furthermore, the striking similarity of low-dimensional population dynamics observed in the motor cortex across mice, non-human primates, and humans suggests that the underlying neural manifolds are deeply conserved dynamical structures across the mammalian evolutionary lineage, potentially reflecting shared bioelectric principles of development. We therefore propose that electric fields act as global dynamical constraints guiding the emergence of evolutionarily conserved neural manifolds and population dynamics. By linking bioelectric field dynamics, brain morphogenesis, and low-dimensional neural activity, this work complements the neural manifold framework and provides a developmental account of how functional neural geometries might emerge from self-organizing biological principles.
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