Abstract

Optogenetics offers a unique method to regulate the activity of select neural circuits. However, the electrophysiological consequences of targeted optogenetic manipulation upon the entire circuit remain poorly understood. Analysis of the sensory-CNS-motor circuit in Drosophila larvae expressing eHpHR and ChR2-XXL revealed unexpected patterns of excitability. Optical stimulation of motor neurons targeted to express eNpHR resulted in inhibition followed by excitation of body wall contraction with repetitive stimulation in intact larvae. In situ preparations with direct electrophysiological measures showed an increased responsiveness to excitatory synaptic activity induced by sensory stimulation within a functional neural circuit. To ensure proper function of eNpHR and ChR2-XXL they were expressed in body wall muscle and direct electrophysiological measurements were obtained. Under eNpHR induced hyperpolarization the muscle remained excitable with increased amplitude of excitatory postsynaptic synaptic potentials. Theoretical models to explain the observations are presented. This study aids in increasing the understanding of the varied possible influences with light activated proteins within intact neural circuits.

Document Type

Article

Publication Date

7-3-2018

Notes/Citation Information

Published in PLOS One, v. 13, no. 7, p. 1-20.

© 2018 Mattingly et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Digital Object Identifier (DOI)

https://doi.org/10.1371/journal.pone.0200107

Funding Information

KW had a summer fellowship from DADD: German Academic Exchange Service, RISE - Program (Research Internships in Science and Engineering) to work in the USA on this project. RLC received funding from the Kentucky Science and Engineering Foundation (KSEF-3712-RDE-019) at the Kentucky Science and Technology Corporation.

Related Content

S1 Video. Larvae expressing ChR2-XXL in muscle are crawling around on the dish when exposed to infra-red light and upon blue light rapidly contract and remain contracted for some time after the blue light is stopped. https://doi.org/10.1371/journal.pone.0200107.s001

S2 Video. When eNpHR is expressed in motor neurons and exposed to yellow light for 15 sec the larvae become flaccid for a short time and then start to crawl. After dark exposure under infa-red the larvae regain full movement after some time. https://doi.org/10.1371/journal.pone.0200107.s002

S3 Video. When eNpHR is expressed in muscle and exposed to yellow light for 15 sec the larvae show slight decreases in body wall locomotion and regain movement rapidly after the yellow light is turned off. https://doi.org/10.1371/journal.pone.0200107.s003

pone.0200107.s001.mp4 (23637 kB)
S1 Video. Larvae expressing ChR2-XXL in muscle are crawling around on the dish when exposed to infra-red light and upon blue light rapidly contract and remain contracted for some time after the blue light is stopped.

pone.0200107.s002.mp4 (28247 kB)
S2 Video. When eNpHR is expressed in motor neurons and exposed to yellow light for 15 sec the larvae become flaccid for a short time and then start to crawl.

pone.0200107.s003.mp4 (33900 kB)
S3 Video. When eNpHR is expressed in muscle and exposed to yellow light for 15 sec the larvae show slight decreases in body wall locomotion and regain movement rapidly after the yellow light is turned off.

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