Voltage-dependent K+ channels improve the energy efficiency of signalling in blowfly photoreceptors
Voltage-dependent conductances in many spiking neurons are tuned to reduce action potential energy consumption, so improving the energy efficiency of spike coding. However, the contribution of voltage-dependent conductances to the energy efficiency of analogue coding, by graded potentials in dendrit...
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| Veröffentlicht in: | Journal of the Royal Society interface 2017-04, Vol.14 (129), p.20160938-20160938 |
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| creator | Heras, Francisco J. H. Anderson, John Laughlin, Simon B. Niven, Jeremy E. |
| description | Voltage-dependent conductances in many spiking neurons are tuned to reduce action potential energy consumption, so improving the energy efficiency of spike coding. However, the contribution of voltage-dependent conductances to the energy efficiency of analogue coding, by graded potentials in dendrites and non-spiking neurons, remains unclear. We investigate the contribution of voltage-dependent conductances to the energy efficiency of analogue coding by modelling blowfly R1-6 photoreceptor membrane. Two voltage-dependent delayed rectifier K+ conductances (DRs) shape the membrane's voltage response and contribute to light adaptation. They make two types of energy saving. By reducing membrane resistance upon depolarization they convert the cheap, low bandwidth membrane needed in dim light to the expensive high bandwidth membrane needed in bright light. This investment of energy in bandwidth according to functional requirements can halve daily energy consumption. Second, DRs produce negative feedback that reduces membrane impedance and increases bandwidth. This negative feedback allows an active membrane with DRs to consume at least 30% less energy than a passive membrane with the same capacitance and bandwidth. Voltage-dependent conductances in other non-spiking neurons, and in dendrites, might be organized to make similar savings. |
| doi_str_mv | 10.1098/rsif.2016.0938 |
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By reducing membrane resistance upon depolarization they convert the cheap, low bandwidth membrane needed in dim light to the expensive high bandwidth membrane needed in bright light. This investment of energy in bandwidth according to functional requirements can halve daily energy consumption. Second, DRs produce negative feedback that reduces membrane impedance and increases bandwidth. This negative feedback allows an active membrane with DRs to consume at least 30% less energy than a passive membrane with the same capacitance and bandwidth. Voltage-dependent conductances in other non-spiking neurons, and in dendrites, might be organized to make similar savings.</description><identifier>ISSN: 1742-5689</identifier><identifier>EISSN: 1742-5662</identifier><identifier>DOI: 10.1098/rsif.2016.0938</identifier><identifier>PMID: 28381642</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>Action potential ; Action Potentials ; Analogue Coding ; Animals ; Bandwidths ; Calliphoridae ; Coding ; Dendrites ; Depolarization ; Diptera - physiology ; Electric Conductivity ; Electric potential ; Energy conservation ; Energy consumption ; Energy conversion efficiency ; Energy efficiency ; Energy Metabolism ; Energy-Aware Bandwidth And Gain Control ; Feedback ; Firing pattern ; Insect Graded-Potential Neuron ; Insect Proteins - physiology ; Ion Channel Gating ; Life Sciences–Engineering interface ; Light adaptation ; Membrane Impedance ; Membrane potential ; Membrane Potentials ; Membrane resistance ; Models, Biological ; Negative Feedback ; Neural coding ; Neurons ; Photoreceptor Cells, Invertebrate - physiology ; Photoreceptors ; Potassium ; Potassium channels (voltage-gated) ; Potassium Channels, Voltage-Gated - physiology ; Potential energy ; Signaling ; Spiking ; Voltage-Sensitive Potassium Conductance</subject><ispartof>Journal of the Royal Society interface, 2017-04, Vol.14 (129), p.20160938-20160938</ispartof><rights>2017 The Author(s)</rights><rights>2017 The Author(s).</rights><rights>Copyright The Royal Society Publishing Apr 2017</rights><rights>2017 The Author(s) 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c591t-4cbff26f8966b5816b09956808bd69d9582fcd9329880be544e5b7481b6e4f393</citedby><cites>FETCH-LOGICAL-c591t-4cbff26f8966b5816b09956808bd69d9582fcd9329880be544e5b7481b6e4f393</cites><orcidid>0000-0001-5946-6313 ; 0000-0001-7786-5254 ; 0000-0003-4659-6543 ; 0000-0001-8124-2359</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5414906/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5414906/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28381642$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Heras, Francisco J. H.</creatorcontrib><creatorcontrib>Anderson, John</creatorcontrib><creatorcontrib>Laughlin, Simon B.</creatorcontrib><creatorcontrib>Niven, Jeremy E.</creatorcontrib><title>Voltage-dependent K+ channels improve the energy efficiency of signalling in blowfly photoreceptors</title><title>Journal of the Royal Society interface</title><addtitle>J. R. Soc</addtitle><addtitle>J R Soc Interface</addtitle><description>Voltage-dependent conductances in many spiking neurons are tuned to reduce action potential energy consumption, so improving the energy efficiency of spike coding. However, the contribution of voltage-dependent conductances to the energy efficiency of analogue coding, by graded potentials in dendrites and non-spiking neurons, remains unclear. We investigate the contribution of voltage-dependent conductances to the energy efficiency of analogue coding by modelling blowfly R1-6 photoreceptor membrane. Two voltage-dependent delayed rectifier K+ conductances (DRs) shape the membrane's voltage response and contribute to light adaptation. They make two types of energy saving. By reducing membrane resistance upon depolarization they convert the cheap, low bandwidth membrane needed in dim light to the expensive high bandwidth membrane needed in bright light. This investment of energy in bandwidth according to functional requirements can halve daily energy consumption. Second, DRs produce negative feedback that reduces membrane impedance and increases bandwidth. This negative feedback allows an active membrane with DRs to consume at least 30% less energy than a passive membrane with the same capacitance and bandwidth. Voltage-dependent conductances in other non-spiking neurons, and in dendrites, might be organized to make similar savings.</description><subject>Action potential</subject><subject>Action Potentials</subject><subject>Analogue Coding</subject><subject>Animals</subject><subject>Bandwidths</subject><subject>Calliphoridae</subject><subject>Coding</subject><subject>Dendrites</subject><subject>Depolarization</subject><subject>Diptera - physiology</subject><subject>Electric Conductivity</subject><subject>Electric potential</subject><subject>Energy conservation</subject><subject>Energy consumption</subject><subject>Energy conversion efficiency</subject><subject>Energy efficiency</subject><subject>Energy Metabolism</subject><subject>Energy-Aware Bandwidth And Gain Control</subject><subject>Feedback</subject><subject>Firing pattern</subject><subject>Insect Graded-Potential Neuron</subject><subject>Insect Proteins - physiology</subject><subject>Ion Channel Gating</subject><subject>Life Sciences–Engineering interface</subject><subject>Light adaptation</subject><subject>Membrane Impedance</subject><subject>Membrane potential</subject><subject>Membrane Potentials</subject><subject>Membrane resistance</subject><subject>Models, Biological</subject><subject>Negative Feedback</subject><subject>Neural coding</subject><subject>Neurons</subject><subject>Photoreceptor Cells, Invertebrate - physiology</subject><subject>Photoreceptors</subject><subject>Potassium</subject><subject>Potassium channels (voltage-gated)</subject><subject>Potassium Channels, Voltage-Gated - physiology</subject><subject>Potential energy</subject><subject>Signaling</subject><subject>Spiking</subject><subject>Voltage-Sensitive Potassium Conductance</subject><issn>1742-5689</issn><issn>1742-5662</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkd2L1DAUxYso7rr66qMEfBGkY5KmafIiLIuriwuCX6-hTW86WTJJTdqR-tebYcZhd0F9uoH8cs65OUXxnOAVwVK8icmaFcWEr7CsxIPilDSMljXn9OHxLORJ8SSlG4yrpqrrx8UJFZUgnNHTQn8PbmoHKHsYwffgJ_TxNdLr1ntwCdnNGMMW0LQGBB7isCAwxmoLXi8oGJTs4FvnrB-Q9ahz4adxCxrXYQoRNIx5pKfFI9O6BM8O86z4dvnu68WH8vrT-6uL8-tS15JMJdOdMZQbITnv6pyvw1Lm9Fh0PZe9rAU1upcVlULgDmrGoO4aJkjHgZlKVmfF273uOHcb6HVeJrZOjdFu2rio0Fp198bbtRrCVtWMMIl5Fnh1EIjhxwxpUhubNDjXeghzUkRi0mRfSv6PCsFyzNxJRl_eQ2_CHPOv7QQFwwJz2mRqtad0DClFMMfcBKtd1WpXtdpVrQ6yL25ve8T_dJuBag_EsGSzkEubllvef5Md_vXq85eryy1hllCpsKgIblj2Ur_suBciTNmUZlA74K70faff9mzZfQ</recordid><startdate>20170401</startdate><enddate>20170401</enddate><creator>Heras, Francisco J. H.</creator><creator>Anderson, John</creator><creator>Laughlin, Simon B.</creator><creator>Niven, Jeremy E.</creator><general>The Royal Society</general><general>The Royal Society Publishing</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QP</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>C1K</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5946-6313</orcidid><orcidid>https://orcid.org/0000-0001-7786-5254</orcidid><orcidid>https://orcid.org/0000-0003-4659-6543</orcidid><orcidid>https://orcid.org/0000-0001-8124-2359</orcidid></search><sort><creationdate>20170401</creationdate><title>Voltage-dependent K+ channels improve the energy efficiency of signalling in blowfly photoreceptors</title><author>Heras, Francisco J. 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| subjects | Action potential Action Potentials Analogue Coding Animals Bandwidths Calliphoridae Coding Dendrites Depolarization Diptera - physiology Electric Conductivity Electric potential Energy conservation Energy consumption Energy conversion efficiency Energy efficiency Energy Metabolism Energy-Aware Bandwidth And Gain Control Feedback Firing pattern Insect Graded-Potential Neuron Insect Proteins - physiology Ion Channel Gating Life Sciences–Engineering interface Light adaptation Membrane Impedance Membrane potential Membrane Potentials Membrane resistance Models, Biological Negative Feedback Neural coding Neurons Photoreceptor Cells, Invertebrate - physiology Photoreceptors Potassium Potassium channels (voltage-gated) Potassium Channels, Voltage-Gated - physiology Potential energy Signaling Spiking Voltage-Sensitive Potassium Conductance |
| title | Voltage-dependent K+ channels improve the energy efficiency of signalling in blowfly photoreceptors |
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