Deploying photons for communication within neuronal networks

Deficiencies in neurotransmission lead to neurological disorders or misinterpretation of perceived threats. To restore defects in cellular communication, we developed a synthetic, photon-assisted synaptic transmission (PhAST) system. PhAST is based on luciferases and channelrhodopsins that enable the transmission of a neuronal state across space, using photons as neurotransmitters. We demonstrate the ability to overcome synaptic barriers and rescue the behavioral deficit of a genetically engineered glutamate mutant with conditional, Ca2+-triggered photon emission between two cognate neurons of the Caenorhabditis elegans nociceptive avoidance circuit. We also deploy these ingredients for asynaptic transmission between two unrelated cells in a sexually dimorphic neuronal network. Functional PhAST could sensitize otherwise poorly responsive males to touch and hence expand the behavioral repertoire. Our study, thus, establishes a powerful framework for complex photon-based communication between neurons in a living animal, that can readily be expanded to synthetic neuronal networks, organoids or non-invasive brain-machine interfaces.