We have discovered that our founding fathers overlooked a bilateral pair of male-specific head interneurons, revealing that the total number of male neurons is 385, not 383. We have termed these neurons the Mystery Cells of the Male (MCMs). Matching the level of characterisation performed by Sulston, White, et al. for all other C. elegans neurons, we have established their identity, lineage origin, connectivity and function.
Through reporter gene analysis, and ultrastructural reconstruction, we find that the MCMs are fully differentiated neurons. The cell bodies of the MCMs are located dorsoanterior to the pharyngeal metacorpus, a region devoid of neuronal cell bodies in the hermaphrodite, and send projections posteriorly into the nerve ring and along the ventral cord. The MCMs express neuronal gene batteries for both electrical and chemical communication. They are born at the early L4 larval stage from a male-specific asymmetric division of the glial amphid socket (AMso) cells. This is the first example of glia acting as neural progenitors in an invertebrate and parallels vertebrate neurogenesis. We find that the male AMso cells are fully differentiated, just like the hermaphrodite AMso cells, before they re-enter the cell cycle. This male-specific division results in self-renewal of the AMso, which does not retract its projection during division, and a cell that transdifferentiates into the MCM neurons.
Reconstruction of the MCM synaptic connectivity through serial reconstruction of electron micrographs reveals a circuit where these neurons create disynaptic pathways in triplet motifs connecting EF (male-specific), AVF, and RIF to AVB. This suggests that the MCMs may incorporate male-specific sensory inputs, such as mate pheromones, into higher-order processing circuits that control chemotactic behaviours. Consistent with this we find that the MCMs are specifically required for sexual conditioning, a mate-experience dependent plasticity in chemotactic responses that trumps the effect of starvation .
1. Sakai, N., Iwata, R., Yokoi, S., Butcher, R. A., Clardy, J., Tomioka, M., and Iino, Y. (2013). A sexually conditioned switch of chemosensory behavior in C. elegans. PLoS ONE 8, e68676.
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