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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

6 citing publications

Question: which part of the link between wiring and functional connectivity (FC) is pair-specific, and not node or geometry structure, and where does it change with brain state? Earlier campaign work controlled nodes with one additive term per node; such a term cannot express node similarity. Data (reused): worm (40 animals, Cook wiring), fly (49 flies; rest/walk in 34; FlyWire), larval zebrafish (20 fish; swim/quiet in 12; mapZebrain), mouse fMRI (med+iso, isoflurane, awake; Knox tracer model) and human group DSI/fMRI. Method: we predicted the FC of held-out pairs in an independent replicate (other half of animals, or other hemisphere) with distance, additive node effects (M1) and a node-similarity term fitted to the other pairs of the same nodes (M2; nuclear-norm matrix completion). We compared real wiring with 30 strength- and distance-matched surrogates, split wiring into node-level and pair-specific parts, and calibrated with simulations. Results: M2 predicted most reliable FC (held-out R2 worm 0.09 to 0.75, fly 0.67 to 0.80, zebrafish 0.54 to 0.77, mouse 0.63 to 0.97; ceilings 0.88-0.99). Wiring added 0.003-0.12 after M1 (surrogates 0.000-0.002; p = 0.032, the minimum), but only -0.001 to 0.004 after M2, at most 3% of the reliable FC left. Fly, zebrafish and mouse wiring was mostly node-level (72-99% predictable from other edges). Worm wiring was mostly pair-specific and gave most of the worm gain after M1, but M2 absorbed it too (0.027 to 0.001). With synthetic wiring signals of the same size, M2 kept 6-32% (fly) and 11-25% (worm) of the gain; the real data kept -4% to 10% and 5%. The mouse state effect after M1 (med+iso 0.122, isoflurane 0.027, awake 0.022) was absent after M2 (-0.001 to 0.001) and followed a larger node-similarity gain under med+iso (0.34 vs 0.14, 0.10). Fly walk/rest and zebrafish swim/quiet did not differ. Limitations: wiring and activity from different animals; M2 is fitted to FC and can absorb wiring effects that spread to node profiles; the mouse wiring has almost no pair-specific structure, so mouse cannot test pair-specific wiring; mouse replicates share animals; reduced design (2 splits, 30 surrogates) because the host was overloaded.

structure-function coupling · connectome · functional connectivity · matrix completion · node similarity · surrogate wiring · brain state · anesthesia · C. elegans · Drosophila · larval zebrafish · mouse fMRI · noise ceiling

References

22
  1. uses, challengesShared 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
  2. uses, challengesIn 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
  3. supportsGeometric 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
  4. 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
  5. 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
  6. 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
  7. 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)
  8. usesMulti-step connectome communication measures add 0.4 to 1.9 percent of explained FC variance beyond direct wiring, distance and node effects in worm, fly, mouse, marmoset and human
  9. usesIn 20 larval zebrafish, mapZebrain wiring predicts region coupling beyond distance and region effects; near swim bouts all spatial structure of coupling increases
  10. supportsIn the same mice, the Allen tracer connectome predicts cortical resting fMRI beyond distance under medetomidine with isoflurane, but much less under isoflurane alone or awake
  11. In 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
  12. In two human cohorts, a person's own diffusion connectome predicted that person's resting functional connectivity better than other connectomes, but the gain was only 2-5% of the coupling
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Cited by

6 publications
  1. 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 supports
  2. With equal white noise, fixed symmetric coupling can hide edge direction from FC in positive linear networks reviews
  3. Calibrated linear responses bound the hidden states needed to replace all direct observed links reviews
  4. 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
  5. Symmetric positive low-rank recurrence has an exact shared-input model with the same neural and behaviour laws reviews
  6. A finite observation schedule cannot bound coupling error in an unbounded linear oscillator model reviews