What an atlas-fitted connectome can and cannot do: evolutionary search over interneuron stimulation in a whole-body C. elegans model

Abstract

The C. elegans connectome is complete, but which behaviours its wiring can produce, and which it cannot, is unknown. We asked this question in a whole-body simulation whose only adaptive element is a learning agent outside the nervous system. The agent may inject current into a short whitelist of interneurons, never into motor neurons or muscles; the 302-neuron OpenWorm c302 network, with dynamics fitted once to a signal-propagation atlas, a literature-based motor layer and a viscoelastic body on agar do the rest. Every hypothesis was pre-registered with its judgement criterion. Stimulating five command and steering interneurons (AVB, AVA, SMDD, SMDV, RIV) was sufficient for chemotaxis to a source 2.5 mm away (91 % of trials; four of five training seeds), whereas stimulating eight sensory neurons was no better than chance, reproducing at the behavioural level the silence of the sensory-to-command step in the fitted network. Evolution rediscovered the pirouette rule, reversing and executing a deep bend when concentration fell, and ablations showed that reversal, deep bend and steering were all necessary. Shuffling the wiring while preserving weights, counts and signs cut performance to a fifth; in the atlas-fitted dynamics this loss was carried by the gap-junction layer. In corridors four body widths wide, corners were passed by a deep bend pressed against the wall, so the dorsal or ventral direction of the bend fixed the direction of the turn. With ventral bends only, right turns almost never occurred and the worm entered the ventral arm of a T-maze first. Because temporal sensing cannot distinguish the arms at a junction, the learned strategy was to enter one arm and reverse when the odour faded; a left-right concentration difference was needed before the bend direction followed the source. The model yields three testable predictions for narrow-maze assays and separates what the wiring contributes to navigation from what sensing and the body must supply.