{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,26]],"date-time":"2026-04-26T23:55:31Z","timestamp":1777247731649,"version":"3.51.4"},"reference-count":65,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2013,10,3]],"date-time":"2013-10-03T00:00:00Z","timestamp":1380758400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1003263","type":"journal-article","created":{"date-parts":[[2013,10,3]],"date-time":"2013-10-03T17:13:21Z","timestamp":1380820401000},"page":"e1003263","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":86,"title":["Balanced Excitatory and Inhibitory Synaptic Currents Promote Efficient Coding and Metabolic Efficiency"],"prefix":"10.1371","volume":"9","author":[{"given":"Biswa","family":"Sengupta","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simon B.","family":"Laughlin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeremy E.","family":"Niven","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2013,10,3]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","unstructured":"Abeles M (1991) Corticonics: neural circuits of the cerebral cortex. Cambridge: Cambridge University Press.","DOI":"10.1017\/CBO9780511574566"},{"key":"ref2","doi-asserted-by":"crossref","unstructured":"Braitenberg V, Sch\u00fcz A (1998) Cortex: statistics and geometry of neuronal connectivity. Berlin; London: Springer.","DOI":"10.1007\/978-3-662-03733-1"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/0301-0082(92)90015-7","article-title":"The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs","volume":"39","author":"J DeFelipe","year":"1992","journal-title":"Prog Neurobiol"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/0959-4388(94)90059-0","article-title":"Noise, neural codes and cortical organization","volume":"4","author":"MN Shadlen","year":"1994","journal-title":"Curr Opin Neurobiol"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"3870","DOI":"10.1523\/JNEUROSCI.18-10-03870.1998","article-title":"The variable discharge of cortical neurons: implications for connectivity, computation, and information coding","volume":"18","author":"MN Shadlen","year":"1998","journal-title":"J Neurosci"},{"key":"ref6","first-page":"113","article-title":"Salient features of synaptic organisation in the cerebral cortex","volume":"26","author":"P Somogyi","year":"1998","journal-title":"Brain Res Brain Res Rev"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1038\/nrn1198","article-title":"The high-conductance state of neocortical neurons in vivo","volume":"4","author":"A Destexhe","year":"2003","journal-title":"Nat Rev Neurosci"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"11569","DOI":"10.1073\/pnas.88.24.11569","article-title":"Synaptic background activity influences spatiotemporal integration in single pyramidal cells","volume":"88","author":"O Bernander","year":"1991","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"1450","DOI":"10.1152\/jn.1998.79.3.1450","article-title":"Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons <italic>in vivo<\/italic>","volume":"79","author":"D Par\u00e9","year":"1998","journal-title":"J Neurophysiol"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1113\/jphysiol.2004.075028","article-title":"Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells","volume":"563","author":"W Mittmann","year":"2005","journal-title":"J Physiol"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1038\/nn1591","article-title":"Synaptic background activity controls spike transfer from thalamus to cortex","volume":"8","author":"J Wolfart","year":"2005","journal-title":"Nat Neurosci"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/nature02116","article-title":"Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex","volume":"426","author":"M Wehr","year":"2003","journal-title":"Nature"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"5280","DOI":"10.1523\/JNEUROSCI.4652-06.2007","article-title":"Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex","volume":"27","author":"M Rudolph","year":"2007","journal-title":"J Neurosci"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1038\/nn1545","article-title":"Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex","volume":"8","author":"WB Wilent","year":"2005","journal-title":"Nat Neurosci"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/S0960-9822(03)00135-0","article-title":"The cost of cortical computation","volume":"13","author":"P Lennie","year":"2003","journal-title":"Curr Biol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1097\/00004647-200110000-00001","article-title":"An energy budget for signaling in the grey matter of the brain","volume":"21","author":"D Attwell","year":"2001","journal-title":"J Cereb Blood Flow Metab"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1038\/jcbfm.2012.35","article-title":"Updated energy budgets for neural computation in the neocortex and cerebellum","volume":"32","author":"C Howarth","year":"2012","journal-title":"J Cereb Blood Flow Metab"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/S0959-4388(00)00237-3","article-title":"Energy as a constraint on the coding and processing of sensory information","volume":"11","author":"SB Laughlin","year":"2001","journal-title":"Current Opinion in Neurobiology"},{"key":"ref19","doi-asserted-by":"crossref","unstructured":"Holden AV (1976) Models of the stochastic activity of neurons: Springer-Verlag.","DOI":"10.1007\/978-3-642-46345-7"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0306-4522(01)00344-X","article-title":"Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons","volume":"107","author":"A Destexhe","year":"2001","journal-title":"Neuroscience"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1038\/9173","article-title":"How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate","volume":"2","author":"M Stemmler","year":"1999","journal-title":"Nat Neurosci"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1038\/14731","article-title":"Information theory and neural coding","volume":"2","author":"A Borst","year":"1999","journal-title":"Nat Neurosci"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1126\/science.275.5307.1805","article-title":"Reproducibility and variability in neural spike trains","volume":"275","author":"RR de Ruyter van Steveninck","year":"1997","journal-title":"Science"},{"key":"ref24","unstructured":"Rieke F, Warland D, de Ruyter, Bialek W (1997) Spikes: Exploring the Neural Code. Cambridge, MA: The MIT Press."},{"key":"ref25","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1038\/236","article-title":"The metabolic cost of neural information","volume":"1","author":"SB Laughlin","year":"1998","journal-title":"Nat Neurosci"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/S0006-3002(89)80038-1","article-title":"The identification of the sodium-pump as the membrane-bound Na<sup>+<\/sup>\/K<sup>+<\/sup>-ATPase: a commentary on \u2018The Influence of Some Cations on an Adenosine Triphosphatase from Peripheral Nerves\u2019","volume":"1000","author":"JC Skou","year":"1989","journal-title":"Biochim Biophys Acta"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"e1000840","DOI":"10.1371\/journal.pcbi.1000840","article-title":"Action potential energy efficiency varies among neuron types in vertebrates and invertebrates","volume":"6","author":"B Sengupta","year":"2010","journal-title":"PLoS Comput Biol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1038\/nn.2276","article-title":"Gating multiple signals through detailed balance of excitation and inhibition in spiking networks","volume":"12","author":"TP Vogels","year":"2009","journal-title":"Nat Neurosci"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1038\/nn.2105","article-title":"Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities","volume":"11","author":"M Okun","year":"2008","journal-title":"Nat Neurosci"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"15760","DOI":"10.1523\/JNEUROSCI.3874-10.2010","article-title":"Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition","volume":"30","author":"J Kremkow","year":"2010","journal-title":"J Neurosci"},{"key":"ref31","doi-asserted-by":"crossref","unstructured":"McDonnell MD, Stocks NG, Pearce CEM, Abbott D (2008) Stochastic resonance: from suprathreshold stochastic resonance to stochastic signal quantization: Cambridge University Press.","DOI":"10.1017\/CBO9780511535239"},{"key":"ref32","first-page":"6103","article-title":"Coherence and stochastic resonance in a two-state system","volume":"61","year":"2000","journal-title":"Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics"},{"key":"ref33","unstructured":"Sengupta B (2011) Information encoding and energy consumption in single neuron models [PhD]. Cambridge, UK: University of Cambridge."},{"key":"ref34","unstructured":"Gibson JR, Connors BW (1995) Neocortex: Chemical and electrical synapses. In: Arbib MA, editor. The handbook of brain theory and neural networks. Cambridge, MA: The MIT Press. pp. 725\u2013732."},{"key":"ref35","doi-asserted-by":"crossref","first-page":"7606","DOI":"10.1523\/JNEUROSCI.17-20-07606.1997","article-title":"Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method","volume":"17","author":"M H\u00e4usser","year":"1997","journal-title":"J Neurosci"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1418","DOI":"10.1016\/S0006-3495(99)76990-0","article-title":"Determining the activation time course of synaptic AMPA receptors from openings of colocalized NMDA receptors","volume":"77","author":"IC Kleppe","year":"1999","journal-title":"Biophys J"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1038\/nrn1625","article-title":"Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors","volume":"6","author":"M Farrant","year":"2005","journal-title":"Nat Rev Neurosci"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.tins.2003.10.010","article-title":"Interneuron Diversity series: Fast in, fast out\u2013temporal and spatial signal processing in hippocampal interneurons","volume":"27","author":"P Jonas","year":"2004","journal-title":"Trends Neurosci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1038\/378075a0","article-title":"Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons","volume":"378","author":"SR Cobb","year":"1995","journal-title":"Nature"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1016\/S0896-6273(02)00593-7","article-title":"Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex","volume":"33","author":"M Hamann","year":"2002","journal-title":"Neuron"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1038\/nature02442","article-title":"Integration of quanta in cerebellar granule cells during sensory processing","volume":"428","author":"P Chadderton","year":"2004","journal-title":"Nature"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/S0896-6273(03)00200-9","article-title":"Shunting inhibition modulates neuronal gain during synaptic excitation","volume":"38","author":"SJ Mitchell","year":"2003","journal-title":"Neuron"},{"key":"ref43","unstructured":"Stemmler M, Sengupta B, Laughlin SB, Niven JE (2012) Energetically Optimal Action Potentials. In: Shawe-Taylor J, Zemel RS, Bartlett P, Pereira FCN, Weinberger KQ, editors. Advances in Neural Information Processing Systems. pp. 1566\u20131574."},{"key":"ref44","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1523\/JNEUROSCI.18-01-00010.1998","article-title":"Input summation by cultured pyramidal neurons is linear and position-independent","volume":"18","author":"S Cash","year":"1998","journal-title":"J Neurosci"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1016\/S0896-6273(03)00148-X","article-title":"Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell","volume":"37","author":"P Poirazi","year":"2003","journal-title":"Neuron"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1038\/nn1206","article-title":"Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites","volume":"7","author":"G Liu","year":"2004","journal-title":"Nat Neurosci"},{"key":"ref47","first-page":"PE44","article-title":"On the fight between excitation and inhibition: location is everything","volume":"2004","author":"BW Mel","year":"2004","journal-title":"Sci STKE"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/35044552","article-title":"Dendritic integration of excitatory synaptic input","volume":"1","author":"JC Magee","year":"2000","journal-title":"Nat Rev Neurosci"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1111\/j.1748-1716.1979.tb06486.x","article-title":"Firing behaviour in a stochastic nerve membrane model based upon the Hodgkin-Huxley equations","volume":"107","author":"E Skaugen","year":"1979","journal-title":"Acta Physiol Scand"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.tins.2012.03.008","article-title":"Experimental evidence for sparse firing in the neocortex","volume":"35","author":"AL Barth","year":"2012","journal-title":"Trends Neurosci"},{"key":"ref51","doi-asserted-by":"crossref","unstructured":"Graham D, Field D (2006) Sparse coding in the neocortex. In: Kaas JH, Krubitzer LA, editors. Evolution of the Nervous Systems: Elsevier.","DOI":"10.1016\/B0-12-370878-8\/00064-1"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1080\/net.12.3.255.270","article-title":"Characterizing the sparseness of neural codes","volume":"12","author":"B Willmore","year":"2001","journal-title":"Network"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1242\/jeb.017574","article-title":"Energy limitation as a selective pressure on the evolution of sensory systems","volume":"211","author":"JE Niven","year":"2008","journal-title":"J Exp Biol"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"e1003157","DOI":"10.1371\/journal.pcbi.1003157","article-title":"Information and efficiency in the nervous system","volume":"9","author":"B Sengupta","year":"2013","journal-title":"PloS Computational Biology"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"R496","DOI":"10.1016\/j.cub.2007.04.024","article-title":"Recurrent neuronal circuits in the neocortex","volume":"17","author":"RJ Douglas","year":"2007","journal-title":"Curr Biol"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1146\/annurev.neuro.27.070203.144152","article-title":"Neuronal circuits of the neocortex","volume":"27","author":"RJ Douglas","year":"2004","journal-title":"Annu Rev Neurosci"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1126\/science.1093173","article-title":"Synfire chains and cortical songs: temporal modules of cortical activity","volume":"304","author":"Y Ikegaya","year":"2004","journal-title":"Science"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1038\/nature09086","article-title":"Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex","volume":"466","author":"M London","year":"2010","journal-title":"Nature"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1113\/jphysiol.1952.sp004764","article-title":"A quantitative description of membrane current and its application to conduction and excitation in nerve","volume":"117","author":"AL Hodgkin","year":"1952","journal-title":"J Physiol"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"011918","DOI":"10.1103\/PhysRevE.81.011918","article-title":"Comparison of Langevin and Markov channel noise models for neuronal signal generation","volume":"81","author":"B Sengupta","year":"2010","journal-title":"Phys Rev E Stat Nonlin Soft Matter Phys"},{"key":"ref61","first-page":"621","article-title":"On the application of information theory to neural spike trains","author":"SP Strong","year":"1998","journal-title":"Proceedings of the Pac Symp Biocomput"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1103\/PhysRevLett.80.197","article-title":"Entropy and information in neural spike trains","volume":"80","author":"SP Strong","year":"1997","journal-title":"Phys Review Letters"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1162\/neco.1995.7.2.399","article-title":"The upward bias in measures of information derived from limited data samples","volume":"7","author":"A Treves","year":"1995","journal-title":"Neural Comput"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/0006-3002(57)90343-8","article-title":"The influence of some cations on an adenosine triphosphatase from peripheral nerves","volume":"23","author":"JC Skou","year":"1957","journal-title":"Biochim Biophys Acta"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1016\/j.neuron.2012.08.019","article-title":"Synaptic energy use and supply","volume":"75","author":"JJ Harris","year":"2012","journal-title":"Neuron"}],"container-title":["PLoS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1003263","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,7,28]],"date-time":"2019-07-28T19:03:16Z","timestamp":1564340596000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1003263"}},"subtitle":[],"editor":[{"given":"Andrew D.","family":"McCulloch","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2013,10,3]]},"references-count":65,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2013,10,3]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1003263","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,10,3]]}}}