Rhodopsin 7 is indispensable for regulating the firing rates of olfactory sensory neurons in response to extracellular field potential changes in Drosophila melanogaster

Although extracellular field potential changes are commonly observed in the nervous systems, it remains controversial if extracellular electrical activity contributes to neural processing or whether it is an epiphenomenon associated with neural activity. We previously reported that the extracellular field potential change in compound eyes in response to light stimulation induces firing rate changes in olfactory sensory neurons in female Drosophila melanogaster. Through further investigation, we found that the extracellular field potential within the olfactory sensillum is regulated by octopaminergic neurons in response to the light stimulation and that rhodopsin 7 mediates the firing rate changes in the olfactory sensory neurons in response to field potential changes in a light-independent manner. Structural analysis suggests a voltage-dependent gating mechanism for rhodopsin 7 to respond to the field potential change. This study reveals that the nervous system actively controls the field potential in response to sensory input, resulting in alteration of behavioral patterns as well as neural firing patterns in a context-dependent manner. Significance statementAlthough extracellular electrical activity has been recorded to diagnose neuropsychiatric disorders, it remains uncertain how it can be controlled by the nervous system. Moreover, it is difficult to investigate how neurons change their excitability by responding to the change in the extracellular field potential, as synaptic communication interferes in the ability to isolate the function of extracellular electrical activity. We here show that the extracellular field potential within the olfactory sensillum in Drosophila melanogaster is actively regulated by octopaminergic neurons in response to sensory input. We also provide evidence that rhodopsin, a major light sensor protein, mediates responses to extracellular electrical signals, resulting in alternation of behavioral patterns as well as neural firing patterns in a context-dependent manner.