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In 40 moving C. elegans, 63% of reliable pair-specific co-activity was locked to six behaviour variables; wiring and transcriptomes explained about 10% of the behaviour-independent rest

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Question: earlier campaign work found that the pair-specific co-activity of worm head neurons (after node effects, soma distance and homologous pairs) is very reliable, but wiring explains only 3-5% of it. What sets this reliable non-wiring part? Approach: in 40 off-food worms (Atanas 2023; 119 NeuroPAL neurons, 4,348 pairs) we divided the co-activity of each animal into a behaviour-locked part (traces predicted out of fold from velocity, reversal, head angle, head angular velocity, pumping and body curvature) and a behaviour-independent part. We measured the share of the reliable pair-specific covariance in each part and how much wiring (Cook 2019), CeNGEN transcriptome similarity, shared transmitter and lineage explain (split-half reliability calibration, leave-one-animal-out jackknife, class-label permutations). Results: the behaviour-locked part held 0.69 [0.65, 0.74] of the reliable pattern (time-shifted behaviour 0.07; 0.63 after detrending with control 0.01; velocity and reversal alone 0.59). It was low-rank (three node factors removed 80%), and similarity of neuron tuning to behaviour, measured in other animals, explained 38% of the total pattern. The behaviour-independent part was still reliable (0.69) and had more dimensions (three factors removed 53%). Wiring explained 2.6% of the total pattern and 4.0% of the behaviour-independent part. Transcriptome similarity added 5.2 points beyond wiring (permutation p = 0.004), but only 1.4 points after control for same class, ganglion and sensory/inter/motor type (p = 0.005). Lineage had no effect. The behaviour-independent coupling was concentrated in nose-tip mechanosensory (IL1, OLQ, OLL) and pharyngeal (NSM, I3) neurons. Eight on-food worms (Dag 2023) agreed in direction with wide intervals (behaviour-locked share 0.50 after detrending); the wiring increase did not replicate. Limitations: correlational; linear behaviour model with no nose-movement data; connectome and class-level transcriptome from other animals; possible cross-talk between near neurons; several controls were added after the first results.

C. elegans · whole-brain calcium imaging · structure-function coupling · functional connectivity · behaviour encoding · connectome · CeNGEN · transcriptome similarity · low-rank structure · NeuroPAL
Neurons and Cognition

References

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  1. 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
  2. supports, usesIn 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
  3. supportsAfter 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. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. In 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)
  12. NSM 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
  13. In two freely moving C. elegans data sets, wiring flow to body-wall muscles predicts how much behaviour explains head neuron activity, but not which body behaviour is encoded
  14. C. elegans neuron classes with shorter connectome walks to body-wall muscle encode locomotion more strongly in two whole-brain data sets, beyond rewired-wiring nulls
  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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  21. doi:10.1016/0012-1606(83)90201-4
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  24. useshttps://github.com/francescorandi/wormneuroatlas/tree/b2e13d88b670efcb3438aeacba2ad4bd6c383933

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