Bulow, Hannes E., Brittin, Christopher A., Nguyen, Ken C.Q., Hall, David H., Tang, Leo T.-H., Jarrell, Travis A., Cook, Steven J., Yakovlev, Maksim, Emmons, Scott W., Wang, Yi, Hobert, Oliver, Bayer, Emily A.
[
International Worm Meeting,
2017]
We present the first whole-animal maps of synaptic connectivity, including anatomical connection strength, of both adult sexes of a species. Our results are based on analyses of legacy and new serial section electron micrographs (EMs) of the C. elegans nervous system and the tissues it innervates. In a graph representation of connectivity, the pathways of information flow can be arranged hierarchically, revealing a largely feed forward structure of shallow (1-5 synapses) depth. Our reconstruction has revealed that muscles and other end-organs are more extensively cross-connected than previously reported. Sensory information converges and diverges widely throughout the fully-connected neural network. The sexes differ not only by the addition of sex-specific neurons and muscles, but also at numerous points in the connectivity of shared neurons. Differences between the hermaphrodite and male reconstructions could be either inter-individual differences or differences due to genetic sex. To distinguish between these possibilities, we examined a subset of 7 synaptic connections that were respectively stronger in the male reconstruction, 4 that were stronger in the hermaphrodite reconstruction, and 4 that were similar, using in vivo trans-synaptic labeling. In each instance, the difference seen in the reconstructions was confirmed in multiple animals. Extrapolating these results to the number of statistically significant differences in the reconstructions, we conclude that there is an unexpectedly large number of sexually dimorphic connections. These connections were mainly located in the nerve ring, and embedded within the connectome at least one synapse away from any sex-specific neuron. Our results showed that AVA receives sex-specific input from ADL, ASH, and AVF in the hermaphrodite, while RIB receives sex-specific input from IL1, IL2, and RIA in the male. AIM, which has been reported to change its neurotransmitter from glutamate in the hermaphrodite to acetylcholine in the male, makes a strong male-specific connection to AIB. These hubs of sex-specific connectivity also maintained the majority of their sex-shared output. Our results suggest that the genetic sex of the nervous system allows for diverse synaptic patterns in a relatively small nervous system.