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      Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission

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          Abstract

          Optogenetic silencing strategies using light-driven ion fluxes permit rapid and effective inhibition of neural activity. Using rodent hippocampal neurons we show that silencing activity with a chloride pump can increase the probability of synaptically-evoked spiking in the period following light-activation, whereas this is not the case for a proton pump. This effect can be accounted for by changes to the GABA A receptor reversal potential and demonstrates an important difference between silencing strategies.

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          High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps

          Brian Chow, Xue Han, Allison S. Dobry … (2010)
          The ability to silence the activity of genetically specified neurons in a temporally precise fashion would open up the ability to investigate the causal role of specific cell classes in neural computations, behaviors, and pathologies. Here we show that members of the class of light-driven outward proton pumps can mediate very powerful, safe, multiple-color silencing of neural activity. The gene archaerhodopsin-31 (Arch) from Halorubrum sodomense enables near-100% silencing of neurons in the awake brain when virally expressed in mouse cortex and illuminated with yellow light. Arch mediates currents of several hundred picoamps at low light powers, and supports neural silencing currents approaching 900 pA at light powers easily achievable in vivo. In addition, Arch spontaneously recovers from light-dependent inactivation, unlike light-driven chloride pumps that enter long-lasting inactive states in response to light. These properties of Arch are appropriate to mediate the optical silencing of significant brain volumes over behaviourally-relevant timescales. Arch function in neurons is well tolerated because pH excursions created by Arch illumination are minimized by self-limiting mechanisms to levels comparable to those mediated by channelrhodopsins2,3 or natural spike firing. To highlight how proton pump ecological and genomic diversity may support new innovation, we show that the blue-green light-drivable proton pump from the fungus Leptosphaeria maculans 4 (Mac) can, when expressed in neurons, enable neural silencing by blue light, thus enabling alongside other developed reagents the potential for independent silencing of two neural populations by blue vs. red light. Light-driven proton pumps thus represent a high-performance and extremely versatile class of “optogenetic” voltage and ion modulator, which will broadly empower new neuroscientific, biological, neurological, and psychiatric investigations.
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            Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution

            Xue Han, Edward Boyden (2007)
            The quest to determine how precise neural activity patterns mediate computation, behavior, and pathology would be greatly aided by a set of tools for reliably activating and inactivating genetically targeted neurons, in a temporally precise and rapidly reversible fashion. Having earlier adapted a light-activated cation channel, channelrhodopsin-2 (ChR2), for allowing neurons to be stimulated by blue light, we searched for a complementary tool that would enable optical neuronal inhibition, driven by light of a second color. Here we report that targeting the codon-optimized form of the light-driven chloride pump halorhodopsin from the archaebacterium Natronomas pharaonis (hereafter abbreviated Halo) to genetically-specified neurons enables them to be silenced reliably, and reversibly, by millisecond-timescale pulses of yellow light. We show that trains of yellow and blue light pulses can drive high-fidelity sequences of hyperpolarizations and depolarizations in neurons simultaneously expressing yellow light-driven Halo and blue light-driven ChR2, allowing for the first time manipulations of neural synchrony without perturbation of other parameters such as spiking rates. The Halo/ChR2 system thus constitutes a powerful toolbox for multichannel photoinhibition and photostimulation of virally or transgenically targeted neural circuits without need for exogenous chemicals, enabling systematic analysis and engineering of the brain, and quantitative bioengineering of excitable cells.
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              Targeting and readout strategies for fast optical neural control in vitro and in vivo.

              Viviana Gradinaru, Kimberly R Thompson, Feng Zhang … (2007)
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 9809671
                Journal ID (pubmed-jr-id): 21092
                Journal ID (nlm-ta): Nat Neurosci
                Journal ID (iso-abbrev): Nat. Neurosci.
                Title: Nature neuroscience
                ISSN (Print): 1097-6256
                ISSN (Electronic): 1546-1726
                Publication date Nihms-submitted: 5 June 2012
                Publication date (Electronic): 24 June 2012
                Publication date PMC-release: 01 February 2013
                Volume: 15
                Issue: 8
                Pages: 1102-1104
                Affiliations
                [1 ]Department of Pharmacology, Oxford University, Oxford, United Kingdom
                Author notes
                Correspondence: Colin J. Akerman, PhD Department of Pharmacology Oxford University Oxford, Mansfield Road, OX1 3QT colin.akerman@ 123456pharm.ox.ac.uk

                Author Contributions J.V.R. and C.J.A. designed research; J.V.R., T.J.E. and L.K. performed experiments, J.V.R. and C.J.A. analyzed data, J.V.R. and C.J.A. wrote the paper.

                Article
                Manuscript ID: UKMS48493
                DOI: 10.1038/nn.3143
                PMC ID: 3428858
                PubMed ID: 22729174
                SO-VID: 60e5a665-73bc-456a-b30f-0540a8007722
                License:

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: Medical Research Council :
                Award ID: G0601503(79899) || MRC_
                Categories
                Subject: Article

                ScienceOpen disciplines: Neurosciences
                Data availability:
                ScienceOpen disciplines: Neurosciences

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