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Review ArticleReview Article

Remote Control of Neuronal Signaling

Sarah C. Rogan and Bryan L. Roth
A. Leslie Morrow, ASSOCIATE EDITOR
Pharmacological Reviews June 2011, 63 (2) 291-315; DOI: https://doi.org/10.1124/pr.110.003020
Sarah C. Rogan
Departments of Pharmacology (S.C.R., B.L.R.) and Psychiatry (B.L.R.), Program in Neuroscience (B.L.R.), Lineberger Comprehensive Cancer Center (B.L.R.), Neurodevelopmental Disorders Research Center (B.L.R.), and Department of Medicinal Chemistry and Natural Products (B.L.R.), University of North Carolina School of Pharmacy, Chapel Hill, North Carolina; and National Institute of Mental Health Psychoactive Drug Screening Program, Chapel Hill, North Carolina (B.L.R.)
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Bryan L. Roth
Departments of Pharmacology (S.C.R., B.L.R.) and Psychiatry (B.L.R.), Program in Neuroscience (B.L.R.), Lineberger Comprehensive Cancer Center (B.L.R.), Neurodevelopmental Disorders Research Center (B.L.R.), and Department of Medicinal Chemistry and Natural Products (B.L.R.), University of North Carolina School of Pharmacy, Chapel Hill, North Carolina; and National Institute of Mental Health Psychoactive Drug Screening Program, Chapel Hill, North Carolina (B.L.R.)
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A. Leslie Morrow
Departments of Pharmacology (S.C.R., B.L.R.) and Psychiatry (B.L.R.), Program in Neuroscience (B.L.R.), Lineberger Comprehensive Cancer Center (B.L.R.), Neurodevelopmental Disorders Research Center (B.L.R.), and Department of Medicinal Chemistry and Natural Products (B.L.R.), University of North Carolina School of Pharmacy, Chapel Hill, North Carolina; and National Institute of Mental Health Psychoactive Drug Screening Program, Chapel Hill, North Carolina (B.L.R.)
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Abstract

A significant challenge for neuroscientists is to determine how both electrical and chemical signals affect the activity of cells and circuits and how the nervous system subsequently translates that activity into behavior. Remote, bidirectional manipulation of those signals with high spatiotemporal precision is an ideal approach to addressing that challenge. Neuroscientists have recently developed a diverse set of tools that permit such experimental manipulation with varying degrees of spatial, temporal, and directional control. These tools use light, peptides, and small molecules to primarily activate ion channels and G protein-coupled receptors (GPCRs) that in turn activate or inhibit neuronal firing. By monitoring the electrophysiological, biochemical, and behavioral effects of such activation/inhibition, researchers can better understand the links between brain activity and behavior. Here, we review the tools that are available for this type of experimentation. We describe the development of the tools and highlight exciting in vivo data. We focus primarily on designer GPCRs (receptors activated solely by synthetic ligands, designer receptors exclusively activated by designer drugs) and microbial opsins (e.g., channelrhodopsin-2, halorhodopsin, Volvox carteri channelrhodopsin) but also describe other novel techniques that use orthogonal receptors, caged ligands, allosteric modulators, and other approaches. These tools differ in the direction of their effect (activation/inhibition, hyperpolarization/depolarization), their onset and offset kinetics (milliseconds/minutes/hours), the degree of spatial resolution they afford, and their invasiveness. Although none of these tools is perfect, each has advantages and disadvantages, which we describe, and they are all still works in progress. We conclude with suggestions for improving upon the existing tools.

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  • This article is available online at http://pharmrev.aspetjournals.org.

    doi:10.1124/pr.110.003020.

  • U.S. Government work not protected by U.S. copyright
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Pharmacological Reviews: 63 (2)
Pharmacological Reviews
Vol. 63, Issue 2
1 Jun 2011
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Review ArticleReview Article

Remote Control of Neuronal Signaling

Sarah C. Rogan and Bryan L. Roth
Pharmacological Reviews June 1, 2011, 63 (2) 291-315; DOI: https://doi.org/10.1124/pr.110.003020

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Review ArticleReview Article

Remote Control of Neuronal Signaling

Sarah C. Rogan and Bryan L. Roth
Pharmacological Reviews June 1, 2011, 63 (2) 291-315; DOI: https://doi.org/10.1124/pr.110.003020
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    • Abstract
    • I. Introduction
    • II. Overview of the Tools and Their Technical Considerations
    • III. Early Approaches
    • IV. Designer G Protein-Coupled Receptors
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