{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T13:03:46Z","timestamp":1792242226245,"version":"4.4.0"},"reference-count":94,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2016,9,2]],"date-time":"2016-09-02T00:00:00Z","timestamp":1472774400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2016,9,2]],"date-time":"2016-09-02T00:00:00Z","timestamp":1472774400000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2016,9,2]],"date-time":"2016-09-02T00:00:00Z","timestamp":1472774400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["R01 NS085006"],"award-info":[{"award-number":["R01 NS085006"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["PHY-0750456"],"award-info":[{"award-number":["PHY-0750456"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>The dynamics of different ionic currents shape the bursting activity of neurons and networks that control motor output. Despite being ubiquitous in all animal cells, the contribution of the Na+\/K+ pump current to such bursting activity has not been well studied. We used monensin, a Na+\/H+ antiporter, to examine the role of the pump on the bursting activity of oscillator heart interneurons in leeches. When we stimulated the pump with monensin, the period of these neurons decreased significantly, an effect that was prevented or reversed when the h-current was blocked by Cs+. The decreased period could also occur if the pump was inhibited with strophanthidin or K+-free saline. Our monensin results were reproduced in model, which explains the pump\u2019s contributions to bursting activity based on Na+ dynamics. Our results indicate that a dynamically oscillating pump current that interacts with the h-current can regulate the bursting activity of neurons and networks.<\/jats:p>","DOI":"10.7554\/elife.19322","type":"journal-article","created":{"date-parts":[[2016,9,1]],"date-time":"2016-09-01T11:59:50Z","timestamp":1472731190000},"source":"Crossref","is-referenced-by-count":52,"title":["Na+\/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches"],"prefix":"10.7554","volume":"5","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2462-5203","authenticated-orcid":true,"given":"Daniel","family":"Kueh","sequence":"first","affiliation":[{"name":"Department of Biology, Emory University, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William H","family":"Barnett","sequence":"additional","affiliation":[{"name":"Neuroscience Institute, Georgia State University, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gennady S","family":"Cymbalyuk","sequence":"additional","affiliation":[{"name":"Neuroscience Institute, Georgia State University, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7135-3469","authenticated-orcid":true,"given":"Ronald L","family":"Calabrese","sequence":"additional","affiliation":[{"name":"Department of Biology, Emory University, Atlanta, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2016,9,2]]},"reference":[{"key":"bib1","doi-asserted-by":"crossref","first-page":"2846","DOI":"10.1523\/JNEUROSCI.09-08-02846.1989","article-title":"A hyperpolarization-activated inward current in heart interneurons of the medicinal leech","volume":"9","author":"Angstadt","year":"1989","journal-title":"Journal of Neuroscience"},{"key":"bib2","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1523\/JNEUROSCI.11-03-00746.1991","article-title":"Calcium currents and graded synaptic transmission between heart interneurons of the leech","volume":"11","author":"Angstadt","year":"1991","journal-title":"Journal of Neuroscience"},{"key":"bib3","doi-asserted-by":"crossref","first-page":"1858","DOI":"10.1152\/jn.1991.66.6.1858","article-title":"Synchronized oscillatory activity in leech neurons induced by calcium channel blockers","volume":"66","author":"Angstadt","year":"1991","journal-title":"Journal of Neurophysiology"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/j.1460-9568.2008.06566.x","article-title":"The H-current secures action potential transmission at high frequencies in rat cerebellar parallel fibers","volume":"29","author":"Baginskas","year":"2009","journal-title":"European Journal of Neuroscience"},{"key":"bib5","doi-asserted-by":"crossref","first-page":"3145","DOI":"10.1152\/jn.1997.77.6.3145","article-title":"Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h)","volume":"77","author":"Bal","year":"1997","journal-title":"Journal of Neurophysiology"},{"key":"bib6","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1152\/jn.1997.77.1.17","article-title":"Pharmacological block of the electrogenic sodium pump disrupts rhythmic bursting induced by strychnine and bicuculline in the neonatal rat spinal cord","volume":"77","author":"Ballerini","year":"1997","journal-title":"Journal of Neurophysiology"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/j.jneumeth.2013.08.021","article-title":"Bistability of silence and seizure-like bursting","volume":"220","author":"Barnett","year":"2013","journal-title":"Journal of Neuroscience Methods"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1113\/jphysiol.1969.sp008880","article-title":"After-effects of nerve impulses on signalling in the central nervous system of the leech","volume":"203","author":"Baylor","year":"1969","journal-title":"The Journal of Physiology"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1007\/s00422-012-0538-y","article-title":"From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander","volume":"107","author":"Bicanski","year":"2013","journal-title":"Biological Cybernetics"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1113\/jphysiol.1973.sp010108","article-title":"The role of electrogenic sodium pumping in the response of smooth muscle to acetylcholine","volume":"228","author":"Bolton","year":"1973","journal-title":"The Journal of Physiology"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"2092","DOI":"10.1073\/pnas.90.5.2092","article-title":"Generation of beta-amyloid in the secretory pathway in neuronal and nonneuronal cells","volume":"90","author":"Busciglio","year":"1993","journal-title":"PNAS"},{"key":"bib12","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1152\/jn.1999.82.1.382","article-title":"Models of respiratory rhythm generation in the pre-B\u00f6tzinger complex. I. Bursting pacemaker neurons","volume":"82","author":"Butera","year":"1999","journal-title":"Journal of Neurophysiology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1007\/BF01870529","article-title":"Charge translocation by the Na,K-pump: I. Kinetics of local field changes studied by time-resolved fluorescence measurements","volume":"121","author":"B\u00fchler","year":"1991","journal-title":"The Journal of Membrane Biology"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1085\/jgp.52.1.1","article-title":"A contribution of an electrogenic Na+ pump to membrane potential in Aplysia neurons","volume":"52","author":"Carpenter","year":"1968","journal-title":"The Journal of General Physiology"},{"key":"bib15","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1242\/jeb.155.1.261","article-title":"Serotonin depresses the after-hyperpolarization through the inhibition of the Na+\/K+ electrogenic pump in T sensory neurones of the leech","volume":"155","author":"Catarsi","year":"1991","journal-title":"The Journal of Experimental Biology"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1196\/annals.1363.021","article-title":"Na+-K+ pump stimulation improves contractility in damaged muscle fibers","volume":"1066","author":"Clausen","year":"2005","journal-title":"Annals of the New York Academy of Sciences"},{"key":"bib17","doi-asserted-by":"crossref","first-page":"L536","DOI":"10.1152\/ajplung.2000.278.3.L536","article-title":"Role of the Na\/H antiport in pH-dependent cell death in pulmonary artery endothelial cells","volume":"278","author":"Cutaia","year":"2000","journal-title":"American Journal of Physiology. Lung Cellular and Molecular Physiology"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/S0925-2312(00)00149-1","article-title":"Oscillatory behaviors in pharmacologically isolated heart interneurons from the medicinal leech","volume":"32-33","author":"Cymbalyuk","year":"2000","journal-title":"Neurocomputing"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/S0925-2312(01)00414-3","article-title":"A model of slow plateau-like oscillations based upon the fast Na+ current in a window mode","volume":"38-40","author":"Cymbalyuk","year":"2001","journal-title":"Neurocomputing"},{"key":"bib20","doi-asserted-by":"crossref","first-page":"10580","DOI":"10.1523\/JNEUROSCI.22-24-10580.2002","article-title":"Bursting in leech heart interneurons: cell-autonomous and network-based mechanisms","volume":"22","author":"Cymbalyuk","year":"2002","journal-title":"Journal of Neuroscience"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"1326","DOI":"10.1126\/science.179.4080.1326","article-title":"Electrogenic sodium pump in squid giant axon","volume":"179","author":"De Weer","year":"1973","journal-title":"Science"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"2242","DOI":"10.1152\/jn.00081.2002","article-title":"Persistent sodium current, membrane properties and bursting behavior of pre-b\u00f6tzinger complex inspiratory neurons in vitro","volume":"88","author":"Del Negro","year":"2002","journal-title":"Journal of Neurophysiology"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1146\/annurev.ph.55.030193.002323","article-title":"Pacemaker mechanisms in cardiac tissue","volume":"55","author":"DiFrancesco","year":"1993","journal-title":"Annual Review of Physiology"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1023\/A:1007548307554","article-title":"Prevention of monensin-induced hyperpolarization in NG108-15 cells","volume":"25","author":"Doebler","year":"2000","journal-title":"Neurochemical Research"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"e1003678","DOI":"10.1371\/journal.pcbi.1003678","article-title":"Identifying crucial parameter correlations maintaining bursting activity","volume":"10","author":"Doloc-Mihu","year":"2014","journal-title":"PLoS Computational Biology"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1113\/jphysiol.1980.sp013298","article-title":"Characterization of the electrogenic sodium pump in cardiac Purkinje fibres","volume":"303","author":"Eisner","year":"1980","journal-title":"The Journal of Physiology"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"4035","DOI":"10.1073\/pnas.77.7.4035","article-title":"Activation of electrogenic Na+\/K+ exchange by extracellular K+ in canine cardiac Purkinje fibers","volume":"77","author":"Gadsby","year":"1980","journal-title":"PNAS"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1113\/jphysiol.1966.sp007918","article-title":"The origin of the post-tetanic hyperpolarization of mammalian motor nerve terminals","volume":"184","author":"Gage","year":"1966","journal-title":"The Journal of Physiology"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1113\/jphysiol.1967.sp008294","article-title":"The behaviour of the sodium pump in red cells in the absence of external potassium","volume":"192","author":"Garrahan","year":"1967","journal-title":"The Journal of Physiology"},{"key":"bib30","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1152\/jn.1983.49.2.509","article-title":"Intracellular alkalinization potentiates slow inward current and prolonged bursting in a molluscan neuron","volume":"49","author":"Gillette","year":"1983","journal-title":"Journal of Neurophysiology"},{"key":"bib31","doi-asserted-by":"crossref","first-page":"1791","DOI":"10.1152\/physrev.2001.81.4.1791","article-title":"Electrophysiology of the sodium-potassium-ATPase in cardiac cells","volume":"81","author":"Glitsch","year":"2001","journal-title":"Physiological Reviews"},{"key":"bib32","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1152\/jn.1992.67.2.318","article-title":"Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crab","volume":"67","author":"Golowasch","year":"1992","journal-title":"Journal of Neurophysiology"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"829","DOI":"10.1016\/0306-4522(90)90112-H","article-title":"Electrogenic pump (Na+\/K(+)-ATPase) activity in rat optic nerve","volume":"37","author":"Gordon","year":"1990","journal-title":"Neuroscience"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1016\/0166-2236(95)80008-P","article-title":"Neural networks that co-ordinate locomotion and body orientation in lamprey","volume":"18","author":"Grillner","year":"1995","journal-title":"Trends in Neurosciences"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"13025","DOI":"10.1523\/JNEUROSCI.0220-13.2013","article-title":"A sodium-pump-mediated afterhyperpolarization in pyramidal neurons","volume":"33","author":"Gulledge","year":"2013","journal-title":"Journal of Neuroscience"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"646","DOI":"10.1016\/S0959-4388(02)00377-X","article-title":"Voltage-sensitive ion channels in rhythmic motor systems","volume":"12","author":"Harris-Warrick","year":"2002","journal-title":"Current Opinion in Neurobiology"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/S0306-4522(01)00167-1","article-title":"Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity","volume":"105","author":"Henze","year":"2001","journal-title":"Neuroscience"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1023\/A:1011216131638","article-title":"A model of a segmental oscillator in the leech heartbeat neuronal network","volume":"10","author":"Hill","year":"2001","journal-title":"Journal of Computational Neuroscience"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/0306-4492(82)90101-0","article-title":"Effects of monensin on the response to low potassium in a molluscan muscle, the radular protractor of busycon canaliculatum","volume":"72","author":"Hill","year":"1982","journal-title":"Comparative Biochemistry and Physiology Part C: Comparative Pharmacology"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1113\/jphysiol.1955.sp005290","article-title":"Active transport of cations in giant axons from Sepia and Loligo","volume":"128","author":"Hodgkin","year":"1955","journal-title":"The Journal of Physiology"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1038\/3721","article-title":"Transduction of temporal patterns by single neurons","volume":"1","author":"Hooper","year":"1998","journal-title":"Nature Neuroscience"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/S0006-8993(00)02822-5","article-title":"Effects of the Na(+)\/H(+) exchanger monensin on intracellular pH in astroglia","volume":"882","author":"Itoh","year":"2000","journal-title":"Brain Research"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/0742-8413(86)90177-5","article-title":"Evidence for the activation of an electrogenic sodium pump in leech retzius neurons following kainate depolarization","volume":"84","author":"Jais","year":"1986","journal-title":"Comparative Biochemistry and Physiology Part C: Comparative Pharmacology"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1113\/jphysiol.1973.sp010158","article-title":"Conductance changes, an electrogenic pump and the hyperpolarization of leech neurones following impulses","volume":"229","author":"Jansen","year":"1973","journal-title":"The Journal of Physiology"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1111\/ejn.12042","article-title":"Sodium and calcium mechanisms of rhythmic bursting in excitatory neural networks of the pre-B\u00f6tzinger complex: a computational modelling study","volume":"37","author":"Jasinski","year":"2013","journal-title":"European Journal of Neuroscience"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1126\/science.1329209","article-title":"Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump","volume":"258","author":"Johnson","year":"1992","journal-title":"Science"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/0010-406X(65)90017-4","article-title":"An electrogenic sodium pump in snail nerve cells","volume":"14","author":"Kerkut","year":"1965","journal-title":"Comparative Biochemistry and Physiology"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"1773","DOI":"10.1523\/JNEUROSCI.3916-07.2008","article-title":"Persistent Na+ and K+-dominated leak currents contribute to respiratory rhythm generation in the pre-B\u00f6tzinger complex in vitro","volume":"28","author":"Koizumi","year":"2008","journal-title":"Journal of Neuroscience"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fncir.2010.00124","article-title":"Outward currents contributing to inspiratory burst termination in preB\u00f6tzinger complex neurons of neonatal mice studied in vitro","volume":"4","author":"Krey","year":"2010","journal-title":"Frontiers in Neural Circuits"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"8870","DOI":"10.1523\/JNEUROSCI.6200-10.2011","article-title":"Ionic dynamics mediate spontaneous termination of seizures and postictal depression state","volume":"31","author":"Krishnan","year":"2011","journal-title":"Journal of Neuroscience"},{"key":"bib51","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00460.2014","article-title":"Electrogenic properties of the Na\u207a\/K\u207a ATPase control transitions between normal and pathological brain states","volume":"113","author":"Krishnan","year":"2015","journal-title":"Journal of Neurophysiology"},{"key":"bib52","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1242\/jeb.65.3.643","article-title":"Rhythmic swimming activity in neurones of the isolated nerve cord of the leech","volume":"65","author":"Kristan","year":"1976","journal-title":"The Journal of Experimental Biology"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"2108","DOI":"10.1242\/jeb.067603","article-title":"Targeting a neuropeptide to discrete regions of the motor arborizations of a single neuron","volume":"215","author":"Kueh","year":"2012","journal-title":"The Journal of Experimental Biology"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1007\/BF01870213","article-title":"Voltage dependence of the rheogenic Na+\/K+ ATPase in the membrane of oocytes of Xenopus laevis","volume":"9","author":"Lafaire","year":"1986","journal-title":"Journal of Membrane Biology"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1016\/j.neuroimage.2011.06.074","article-title":"Optical probing of sodium dynamics in neurons and astrocytes","volume":"58","author":"Lamy","year":"2011","journal-title":"NeuroImage"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"2580","DOI":"10.1073\/pnas.76.6.2580","article-title":"Mechanism of monensin-induced hyperpolarization of neuroblastoma-glioma hybrid NG108-15","volume":"76","author":"Lichtshtein","year":"1979","journal-title":"PNAS"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.neuroscience.2004.06.028","article-title":"Acetyl-L-carnitine induces a sustained potentiation of the afterhyperpolarization","volume":"128","author":"Lombardo","year":"2004","journal-title":"Neuroscience"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1126\/science.166.3905.613","article-title":"Seawater teleosts: evidence for a sodium-potassium exchange in the branchial sodium-excreting pump","volume":"166","author":"Maetz","year":"1969","journal-title":"Science"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"R986","DOI":"10.1016\/S0960-9822(01)00581-4","article-title":"Central pattern generators and the control of rhythmic movements","volume":"11","author":"Marder","year":"2001","journal-title":"Current Biology"},{"key":"bib60","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1152\/physrev.1996.76.3.687","article-title":"Principles of rhythmic motor pattern generation","volume":"76","author":"Marder","year":"1996","journal-title":"Physiological Reviews"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"e1002930","DOI":"10.1371\/journal.pcbi.1002930","article-title":"High prevalence of multistability of rest states and bursting in a database of a model neuron","volume":"9","author":"Marin","year":"2014","journal-title":"PLoS Computational Biology"},{"key":"bib62","doi-asserted-by":"publisher","first-page":"1572","DOI":"10.1152\/jn.00336.2001","article-title":"Phase relationships between segmentally organized oscillators in the leech heartbeat pattern generating network","volume":"87","author":"Masino","year":"2002","journal-title":"Journal of Neurophysiology"},{"key":"bib63","first-page":"H488","article-title":"Dependence of Na-K pump current on internal Na+ in mammalian cardiac myocytes","volume":"259","author":"Mogul","year":"1990","journal-title":"The American Journal of Physiology"},{"key":"bib64","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1113\/jphysiol.1966.sp008078","article-title":"Post-tetanic hyperpolarization and electrogenic Na pump in stretch receptor neurone of crayfish","volume":"187","author":"Nakajima","year":"1966","journal-title":"The Journal of Physiology"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"2992","DOI":"10.1152\/jn.00877.2007","article-title":"A central pattern generator producing alternative outputs: pattern, strength, and dynamics of premotor synaptic input to leech heart motor neurons","volume":"98","author":"Norris","year":"2007","journal-title":"Journal of Neurophysiology"},{"key":"bib66","doi-asserted-by":"crossref","first-page":"4958","DOI":"10.1523\/JNEUROSCI.16-16-04958.1996","article-title":"Calabrese RLActivation of intrinsic and synaptic currents in leech heart interneurons by realistic waveforms","volume":"16","author":"Olsen","year":"1996","journal-title":"Jounal of Neuroscience"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"2857","DOI":"10.1152\/jn.00582.2006","article-title":"Hybrid systems analysis of the control of burst duration by low-voltage-activated calcium current in leech heart interneurons","volume":"96","author":"Olypher","year":"2006","journal-title":"Journal of Neurophysiology"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1007\/BF00191850","article-title":"A persistent sodium current contributes to oscillatory activity in heart interneurons of the medicinal leech","volume":"175","author":"Opdyke","year":"1994","journal-title":"Journal of Comparative Physiology A"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1038\/nn.2444","article-title":"Spike integration and cellular memory in a rhythmic network from Na+\/K+ pump current dynamics","volume":"13","author":"Pulver","year":"2010","journal-title":"Nature Neuroscience"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1113\/jphysiol.1968.sp008502","article-title":"On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations","volume":"196","author":"Rang","year":"1968","journal-title":"The Journal of Physiology"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/0006-8993(94)90039-6","article-title":"Potassium and calcium channel dependence of bursting in cultured neuronal networks","volume":"643","author":"Rhoades","year":"1994","journal-title":"Brain Research"},{"key":"bib72","first-page":"327","volume-title":"Current Topics in Bioenergetics, Vol. 4","author":"Ritchie","year":"1971"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1007\/s004240050668","article-title":"Axonal and glial currents activated during the post-tetanic hyperpolarization in non-myelinated nerve","volume":"436","author":"Robert","year":"1998","journal-title":"Pfl\u00fcgers Archiv"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1007\/s00422-003-0447-1","article-title":"Intrinsic bursting activity in the pre-B\u00f6tzinger complex: role of persistent sodium and potassium currents","volume":"90","author":"Rybak","year":"2004","journal-title":"Biological Cybernetics"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1113\/jphysiol.1996.sp021126","article-title":"Sodium--potassium pump current in rabbit sino-atrial node cells","volume":"490","author":"Sakai","year":"1996","journal-title":"The Journal of Physiology"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/S0306-3623(98)00271-7","article-title":"Pharmacological actions of monovalent ionophores on spontaneously beating rabbit sino-atrial nodal cells","volume":"33","author":"Satoh","year":"1999","journal-title":"General Pharmacology: The Vascular System"},{"key":"bib77","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1242\/jeb.171.1.329","article-title":"Evidence that acetylcholine is an inhibitory transmitter of heart interneurons in the leech","volume":"171","author":"Schmidt","year":"1992","journal-title":"The Journal of Experimental Biology"},{"key":"bib78","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1523\/JNEUROSCI.12-02-00525.1992","article-title":"Modulatory effects of FMRF-NH2 on outward currents and oscillatory activity in heart interneurons of the medicinal leech","volume":"12","author":"Simon","year":"1992","journal-title":"Journal of Neuroscience"},{"key":"bib79","first-page":"E834","article-title":"Na+-H+ antiport and monensin effects on cytosolic pH and iodide transport in FRTL-5 rat thyroid cells","volume":"262","author":"Smallridge","year":"1992","journal-title":"The American Journal of Physiology"},{"key":"bib80","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1126\/science.162.3852.456","article-title":"A role for the sodium pump in photoreception in Limulus","volume":"162","author":"Smith","year":"1968","journal-title":"Science"},{"key":"bib81","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1085\/jgp.57.2.125","article-title":"Inhibition of impulse activity in a sensory neuron by an electrogenic pump","volume":"57","author":"Sokolove","year":"1971","journal-title":"The Journal of General Physiology"},{"key":"bib82","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1113\/jphysiol.2003.048058","article-title":"Unmyelinated axons in the rat hippocampus hyperpolarize and activate an H current when spike frequency exceeds 1 Hz","volume":"552","author":"Soleng","year":"2003","journal-title":"The Journal of Physiology"},{"key":"bib83","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1113\/jphysiol.1991.sp018745","article-title":"Two inward currents and the transformation of low-frequency oscillations of rat and cat thalamocortical cells","volume":"441","author":"Soltesz","year":"1991","journal-title":"The Journal of Physiology"},{"key":"bib84","doi-asserted-by":"publisher","first-page":"5427","DOI":"10.1523\/JNEUROSCI.4449-03.2004","article-title":"Using a hybrid neural system to reveal regulation of neuronal network activity by an intrinsic current","volume":"24","author":"Sorensen","year":"2004","journal-title":"Journal of Neuroscience"},{"key":"bib85","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1152\/physrev.1972.52.3.563","article-title":"Electrogenic sodium pump in nerve and muscle cells","volume":"52","author":"Thomas","year":"1972","journal-title":"Physiological Reviews"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1113\/jphysiol.1972.sp009694","article-title":"Intracellular sodium activity and the sodium pump in snail neurones","volume":"220","author":"Thomas","year":"1972","journal-title":"The Journal of Physiology"},{"key":"bib87","doi-asserted-by":"publisher","first-page":"3938","DOI":"10.1152\/jn.00340.2005","article-title":"Myomodulin increases Ih and inhibits the NA\/K pump to modulate bursting in leech heart interneurons","volume":"94","author":"Tobin","year":"2005","journal-title":"Journal of Neurophysiology"},{"key":"bib88","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/0014-2999(90)94195-4","article-title":"Electrophysiological effects of monensin, a sodium ionophore, on cardiac Purkinje fibers","volume":"190","author":"Tsuchida","year":"1990","journal-title":"European Journal of Pharmacology"},{"key":"bib89","doi-asserted-by":"crossref","first-page":"6946","DOI":"10.1523\/JNEUROSCI.15-10-06946.1995","article-title":"Coupling potentials in CA1 neurons during calcium-free-induced field burst activity","volume":"15","author":"Valiante","year":"1995","journal-title":"Journal of Neuroscience"},{"key":"bib90","doi-asserted-by":"publisher","first-page":"2024","DOI":"10.1152\/jn.00361.2012","article-title":"Intracellular Na(+) and metabolic modulation of Na\/K pump and excitability in the rat suprachiasmatic nucleus neurons","volume":"108","author":"Wang","year":"2012","journal-title":"Journal of Neurophysiology"},{"key":"bib91","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1152\/jn.00856.2013","article-title":"Variation in motor output and motor performance in a centrally generated motor pattern","volume":"112","author":"Wenning","year":"2014","journal-title":"Journal of Neurophysiology"},{"key":"bib92","doi-asserted-by":"publisher","first-page":"16188","DOI":"10.1038\/srep16188","article-title":"Mechanisms underlying the activity-dependent regulation of locomotor network performance by the Na+ pump","volume":"5","author":"Zhang","year":"2015","journal-title":"Scientific Reports"},{"key":"bib93","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1016\/j.cub.2012.01.058","article-title":"Short-term memory of motor network performance via activity-dependent potentiation of Na+\/K+ pump function","volume":"22","author":"Zhang","year":"2012","journal-title":"Current Biology"},{"key":"bib94","doi-asserted-by":"crossref","first-page":"9059","DOI":"10.1523\/JNEUROSCI.23-27-09059.2003","article-title":"Overexpression of a hyperpolarization-activated cation current (Ih) channel gene modifies the firing activity of identified motor neurons in a small neural network","volume":"23","author":"Zhang","year":"2003","journal-title":"Journal of Neuroscience"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/19322\/elife-19322-v1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/19322\/elife-19322-v1.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/19322","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T20:56:34Z","timestamp":1697057794000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/19322"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,9,2]]},"references-count":94,"alternative-id":["10.7554\/eLife.19322"],"URL":"https:\/\/doi.org\/10.7554\/elife.19322","archive":["CLOCKSS"],"relation":{"is-supplemented-by":[{"id-type":"doi","id":"10.5061\/dryad.fr1r2","asserted-by":"subject"}],"has-review":[{"id-type":"doi","id":"10.7554\/eLife.19322.016","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.19322.015","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.726706373.793525625","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,9,2]]},"article-number":"e19322"}}