The question of how neurons are instructed to wire into specific synaptic pathways and networks remains one of the key unsolved problems in the neurosciences. While molecules have been discovered that are required for synaptic wiring, no coherent theme or logic for neuronal wiring along synaptic pathways and entire circuits has yet emerged. Over the last many years, my lab has generated extensive molecular maps of the entire C. elegans nervous system, with a particular focus on systems-wide neurotransmitter maps. We used these maps to identify transcription factors that control neurotransmitter specification throughout most of the C.elegans nervous system. Viewed in conjunction with the long- known connectome of the C.elegans nervous system, our findings led us to propose the existence of a broadly used organizational principle that may help to explain how neurons wire into synaptic pathways and circuits. Specifically, we have found that transcription factors that are re-iteratively used in distinct neuron types to specify neurotransmitter identity often act in synaptically connected neurons. We propose that these transcription factors act as “connectivity transcription factors” that not only specify neurotransmitter identity but also instruct the patterns of synaptic connectivity of neurons in the context of specific neuronal circuits. The notion that the expression patterns of neurotransmitter identity-specifying transcription factors may predict synaptic connectivity may have a fundamental impact on delineating neuronal circuitries in more complex nervous systems and may ultimately guide the reverse engineering of neuronal circuits.
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