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Behaviour-locked covariance carried 71% of reliable pair-specific coactivity in 40 moving C. elegans and 47-52% in 22 larval zebrafish; wiring explained under 8% of the remainder

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Question: earlier campaign work found that pair-specific functional connectivity (FC) is highly reliable, but wiring explains only 5-24% of it after node and distance effects. What sets the large, reliable, non-wiring part? Approach: in each animal, a cross-validated ridge model predicted each neuron or region from measured behaviour (worm: velocity, reversal, head bending, pumping; zebrafish: swims and dark flashes). The correlation of z-scored traces then splits exactly into a behaviour-locked part, a residual part and a cross term. After node fixed effects and distance terms were removed, split halves of animals gave the share of the reliable pair-specific coactivity that each part carries, and the correlation of wiring with the noise-free pattern of each part (rho). Nulls: time-shifted behaviour, node-label permutation and a simulation with known truth; leave-one-animal-out jackknife intervals. Results: in 40 freely moving off-food worms (Atanas 2023; 107 neurons, 4,293 pairs), the behaviour-locked part carried 0.712 (0.688-0.736) of the reliable pair pattern (time-shifted null 0.027). Locomotion features alone carried 0.708. Rank-3 node factors of this part, fit on independent animals, removed 70% of the reliable pattern. Anatomy (gap junctions, chemical synapses, shared input and output, contact) explained 1.9% of the locked part (rho 0.138) and 5.1% of the residual part (rho 0.226); with class, transmitter, type and lineage added, 7.7% of the residual. In 8 on-food worms (Dag 2023) the locked share was 0.490 (0.372-0.608; null 0.092), with more weight on pumping. In 22 larval zebrafish (Legare 2025; 65 regions) the swim- and flash-locked part carried 0.466 (0.397-0.535; null 0.048), 0.520 in 16 swimmers; there, locked and residual patterns had the same shape (calibrated r 0.72) and anatomy related to both equally (rho 0.34, 0.39). In simulation the share estimate was conservative and rho was accurate. Limitations: a linear behaviour model cannot separate activity that drives behaviour from activity that follows it, and it misses unmeasured behaviour; connectomes and activity come from different animals; the on-food cohort is small; zebrafish data are region averages at 1 volume/s; no fly or mouse data; analyses chosen after earlier campaign results.

structure-function coupling · functional connectivity · C. elegans · larval zebrafish · behaviour encoding · connectome · split-half reliability · variance decomposition
Neurons and Cognition

References

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  1. uses, supportsIn 40 worms, 50 flies and 22 larval zebrafish, wiring explained 2-24% of the reliable pair-specific coupling after node and distance controls; the link was pair-specific, and only swimming changed it
  2. supportsWiring explained 5% (worm), 11% (zebrafish) and 24% (fly) of reliable pair-specific FC; much fly and mouse wiring signal was a smooth spatial field; of three behaviours only swimming raised the share
  3. After node similarity is controlled, wiring adds at most 0.004 held-out R2 to functional coupling in worm, fly, zebrafish, mouse and human data; the anesthesia effect on mouse coupling is node-level
  4. Shared input predicts functional coupling beyond direct wiring, distance and node effects in 40 worms, 49 flies and 79 anesthetized mice; the best polysynaptic measure is different in each animal
  5. In fly, mouse and human data, surrogate wiring with matched node strengths and distances reproduced 48-100% of the FC gain of indirect-path measures; a large specific gain stayed only in sedated mouse
  6. Geometric eigenmodes beat connectome eigenmodes for FC in fly, mouse and human but not in worm; simulated connectome-driven FC with spatial blur gives the same result
  7. In 48 freely moving C. elegans, smooth wiring eigenmodes held more head activity variance than rewired graphs, but not more than a distance-only graph with the same edge count
  8. FlyWire wiring predicts neuropil calcium correlations beyond distance in 50 flies; walking and rest coupling agree after global-signal removal; transmitter-matched wiring adds no gain
  9. Single-neuron axon co-innervation predicted spike correlations between 30 mouse cortical areas, but real collateral patterns did not predict better than source-matched shuffles at 100 ms
  10. supportsIn larval zebrafish, a single-neuron projectome predicts region-level trial-residual coupling beyond distance and region effects, but not stimulus-locked coupling (25 regions, 11 fish)
  11. usesNSM serotonergic state did not change wiring coupling of co-activity in 40 off-food C. elegans; an on-food decrease in 8 worms matched a drop in activity variance
  12. usesIn 40 freely moving C. elegans, gap junctions predict pairwise co-activity after controls for neurite contact, soma distance and per-neuron effects; chemical synapse weight does not
  13. usesIn 20 larval zebrafish, mapZebrain wiring predicts region coupling beyond distance and region effects; near swim bouts all spatial structure of coupling increases
  14. Gap junction weight had a positive co-activity link after three reference population modes were removed in two worm cohorts
  15. Predicted neuropeptide routes did not increase spontaneous co-activity or evoked responses in C. elegans after wiring and neuron controls; a small negative co-activity link was not matching-specific
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