{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,28]],"date-time":"2026-07-28T15:24:26Z","timestamp":1785252266232,"version":"3.55.0"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1008573","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,1,29]],"date-time":"2021-01-29T00:00:00Z","timestamp":1611878400000}}],"reference-count":67,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2021,1,19]],"date-time":"2021-01-19T00:00:00Z","timestamp":1611014400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["KI-835\/3"],"award-info":[{"award-number":["KI-835\/3"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["CRC 1080-A01"],"award-info":[{"award-number":["CRC 1080-A01"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"BMBF","award":["031L0229"],"award-info":[{"award-number":["031L0229"]}]},{"DOI":"10.13039\/100009103","name":"Von-Behring-R\u00f6ntgen-Stiftung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009103","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>\n                    The impact of GABAergic transmission on neuronal excitability depends on the Cl\n                    <jats:sup>-<\/jats:sup>\n                    -gradient across membranes. However, the Cl\n                    <jats:sup>-<\/jats:sup>\n                    -fluxes through GABA\n                    <jats:sub>A<\/jats:sub>\n                    receptors alter the intracellular Cl\n                    <jats:sup>-<\/jats:sup>\n                    concentration ([Cl\n                    <jats:sup>-<\/jats:sup>\n                    ]\n                    <jats:sub>i<\/jats:sub>\n                    ) and in turn attenuate GABAergic responses, a process termed ionic plasticity. Recently it has been shown that coincident glutamatergic inputs significantly affect ionic plasticity. Yet how the [Cl\n                    <jats:sup>-<\/jats:sup>\n                    ]\n                    <jats:sub>i<\/jats:sub>\n                    changes depend on the properties of glutamatergic inputs and their spatiotemporal relation to GABAergic stimuli is unknown. To investigate this issue, we used compartmental biophysical models of Cl\n                    <jats:sup>-<\/jats:sup>\n                    dynamics simulating either a simple ball-and-stick topology or a reconstructed CA3 neuron. These computational experiments demonstrated that glutamatergic co-stimulation enhances GABA receptor-mediated Cl\n                    <jats:sup>-<\/jats:sup>\n                    influx at low and attenuates or reverses the Cl\n                    <jats:sup>-<\/jats:sup>\n                    efflux at high initial [Cl\n                    <jats:sup>-<\/jats:sup>\n                    ]\n                    <jats:sub>i<\/jats:sub>\n                    . The size of glutamatergic influence on GABAergic Cl\n                    <jats:sup>-<\/jats:sup>\n                    -fluxes depends on the conductance, decay kinetics, and localization of glutamatergic inputs. Surprisingly, the glutamatergic shift in GABAergic Cl\n                    <jats:sup>-<\/jats:sup>\n                    -fluxes is invariant to latencies between GABAergic and glutamatergic inputs over a substantial interval. In agreement with experimental data, simulations in a reconstructed CA3 pyramidal neuron with physiological patterns of correlated activity revealed that coincident glutamatergic synaptic inputs contribute significantly to the activity-dependent [Cl\n                    <jats:sup>-<\/jats:sup>\n                    ]\n                    <jats:sub>i<\/jats:sub>\n                    changes. Whereas the influence of spatial correlation between distributed glutamatergic and GABAergic inputs was negligible, their temporal correlation played a significant role. In summary, our results demonstrate that glutamatergic co-stimulation had a substantial impact on ionic plasticity of GABAergic responses, enhancing the attenuation of GABAergic inhibition in the mature nervous systems, but suppressing GABAergic [Cl\n                    <jats:sup>-<\/jats:sup>\n                    ]\n                    <jats:sub>i<\/jats:sub>\n                    changes in the immature brain. Therefore, glutamatergic shift in GABAergic Cl\n                    <jats:sup>-<\/jats:sup>\n                    -fluxes should be considered as a relevant factor of short-term plasticity.\n                  <\/jats:p>","DOI":"10.1371\/journal.pcbi.1008573","type":"journal-article","created":{"date-parts":[[2021,1,19]],"date-time":"2021-01-19T13:44:36Z","timestamp":1611063876000},"page":"e1008573","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["Coincident glutamatergic depolarizations enhance GABAA receptor-dependent Cl- influx in mature and suppress Cl- efflux in immature neurons"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6936-4094","authenticated-orcid":true,"given":"Aniello","family":"Lombardi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Jedlicka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heiko J.","family":"Luhmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8204-3984","authenticated-orcid":true,"given":"Werner","family":"Kilb","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,1,19]]},"reference":[{"key":"pcbi.1008573.ref001","first-page":"59","article-title":"The cellular, molecular and ionic basis of GABA(A) receptor signalling","volume":"160","author":"M Farrant","year":"2007","journal-title":"ProgBrain Res"},{"key":"pcbi.1008573.ref002","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fnmol.2019.00168","article-title":"From hiring to firing: Activation of inhibitory neurons and their recruitment in behavior","volume":"12","author":"OK Swanson","year":"2019","journal-title":"Front Mol Neurosci"},{"key":"pcbi.1008573.ref003","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1016\/j.neuron.2009.03.003","article-title":"Cation-chloride cotransporters and neuronal function","volume":"61","author":"P Blaesse","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1008573.ref004","first-page":"27","article-title":"Kinetic properties of Cl- uptake mediated by Na +-dependent K+-2Cl- cotransport in immature rat neocortical neurons","author":"K Achilles","year":"2007","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref005","article-title":"Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1","author":"J Yamada","year":"2004","journal-title":"J Physiol"},{"key":"pcbi.1008573.ref006","doi-asserted-by":"crossref","first-page":"35","DOI":"10.3389\/fncel.2012.00035","article-title":"Refuting the challenges of the developmental shift of polarity of GABA actions: GABA more exciting than ever","volume":"6","author":"Y Ben Ari","year":"2012","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref007","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1111\/j.1460-9568.2011.07878.x","article-title":"Electrical activity patterns and the functional maturation of the neocortex","volume":"34","author":"W Kilb","year":"2011","journal-title":"Eur J Neurosci"},{"key":"pcbi.1008573.ref008","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fncel.2017.00379","article-title":"Modulation of neocortical development by early neuronal activity: Physiology and pathophysiology","volume":"11","author":"S Kirischuk","year":"2017","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref009","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1113\/jphysiol.2006.107086","article-title":"The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus","volume":"573","author":"ST Sipila","year":"2006","journal-title":"J Physiol"},{"key":"pcbi.1008573.ref010","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1113\/jphysiol.2004.077495","article-title":"Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII","volume":"562","author":"C Rivera","year":"2005","journal-title":"J Physiol"},{"key":"pcbi.1008573.ref011","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/fnsyn.2012.00005","article-title":"Short-term ionic plasticity at GABAergic synapses","volume":"4","author":"JV Raimondo","year":"2012","journal-title":"Front Synaptic Neurosci"},{"key":"pcbi.1008573.ref012","doi-asserted-by":"crossref","first-page":"9613","DOI":"10.1523\/JNEUROSCI.1488-05.2005","article-title":"Differential maturation of GABA action and anion reversal potential in spinal lamina I neurons: impact of chloride extrusion capacity","volume":"25","author":"M Cordero-Erausquin","year":"2005","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref013","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1126\/science.7638623","article-title":"Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors","volume":"269","author":"KJ Staley","year":"1995","journal-title":"Science"},{"key":"pcbi.1008573.ref014","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/S0896-6273(00)00056-8","article-title":"A genetically encoded ratiometric indicator for chloride: Capturing chloride transients in cultured hippocampal neurons","volume":"27","author":"T Kuner","year":"2000","journal-title":"Neuron"},{"key":"pcbi.1008573.ref015","doi-asserted-by":"crossref","first-page":"2412","DOI":"10.1152\/jn.2001.85.6.2412","article-title":"Dynamic modulation of excitation and inhibition during stimulation at gamma and beta frequencies in the CA1 hippocampal region","volume":"85","author":"E Bracci","year":"2001","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref016","doi-asserted-by":"crossref","first-page":"2752","DOI":"10.1152\/jn.00142.2003","article-title":"Synaptically activated Cl- accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons","volume":"90","author":"Y Isomura","year":"2003","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref017","doi-asserted-by":"crossref","first-page":"420","DOI":"10.3389\/fncel.2018.00420","article-title":"Giant depolarizing potentials trigger transient changes in the intracellular Cl\u2014concentration in CA3 pyramidal neurons of the immature mouse hippocampus","volume":"12","author":"A Lombardi","year":"2018","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref018","first-page":"461","article-title":"Activity-dependent scaling of GABAergic excitation by dynamic Cl\u2014changes in Cajal-Retzius cells","author":"SN Kolbaev","year":"2011","journal-title":"Pflugers Arch Eur J Physiol"},{"key":"pcbi.1008573.ref019","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0094559","article-title":"Activity Blockade and GABA(A) Receptor Blockade Produce Synaptic Scaling through Chloride Accumulation in Embryonic Spinal Motoneurons and Interneurons","volume":"9","author":"C Lindsly","year":"2014","journal-title":"PLoS One"},{"key":"pcbi.1008573.ref020","doi-asserted-by":"crossref","first-page":"139","DOI":"10.33549\/physiolres.930764","article-title":"Inhibitory transmission, activity-dependent ionic changes and neuronal network oscillations","volume":"55","author":"P Jedli\u010dka","year":"2006","journal-title":"Physiological Research"},{"key":"pcbi.1008573.ref021","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1152\/jn.00162.2005","article-title":"Chloride-sensitive MEQ fluorescence in chick embryo motoneurons following manipulations of chloride and during spontaneous network activity","volume":"95","author":"N Chub","year":"2006","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref022","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1152\/jn.90986.2008","article-title":"NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons","volume":"101","author":"C Gonzalez-Islas","year":"2009","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref023","first-page":"34","volume-title":"Current Opinion in Neurobiology","author":"K Kaila","year":"2014"},{"key":"pcbi.1008573.ref024","doi-asserted-by":"crossref","first-page":"728395","DOI":"10.1155\/2011\/728395","article-title":"Spatial and Temporal Dynamics in the Ionic Driving Force for GABA(A) Receptors","volume":"2011","author":"R Wright","year":"2011","journal-title":"Neural Plast."},{"key":"pcbi.1008573.ref025","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1002\/hipo.20804","article-title":"Activity-dependent intracellular chloride accumulation and diffusion controls GABAA receptor-mediated synaptic transmission","volume":"21","author":"P Jedlicka","year":"2011","journal-title":"Hippocampus"},{"key":"pcbi.1008573.ref026","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.39575","article-title":"Biophysical models reveal the relative importance of transporter proteins and impermeant anions in chloride homeostasis","volume":"7","author":"KM D\u00fcsterwald","year":"2018","journal-title":"Elife"},{"key":"pcbi.1008573.ref027","doi-asserted-by":"crossref","first-page":"e1002149","DOI":"10.1371\/journal.pcbi.1002149","article-title":"Efficacy of Synaptic Inhibition Depends on Multiple, Dynamically Interacting Mechanisms Implicated in Chloride Homeostasis","volume":"7","author":"N Doyon","year":"2011","journal-title":"Plos Comput Biol"},{"key":"pcbi.1008573.ref028","doi-asserted-by":"crossref","first-page":"11619","DOI":"10.1523\/JNEUROSCI.4228-15.2016","article-title":"Reduced efficacy of the KCC2 cotransporter promotes epileptic oscillations in a subiculum network model","volume":"36","author":"A Buchin","year":"2016","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref029","doi-asserted-by":"crossref","first-page":"23196","DOI":"10.1038\/srep23196","article-title":"Spines slow down dendritic chloride diffusion and affect short-term ionic plasticity of GABAergic inhibition","volume":"6","author":"N Mohapatra","year":"2016","journal-title":"Sci Rep"},{"key":"pcbi.1008573.ref030","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/ijms20061416","article-title":"Interactions between membrane resistance, GABA-A receptor properties, bicarbonate dynamics and Cl\u2212-transport shape activity-dependent changes of intracellular Cl\u2212 concentration.","volume":"20","author":"A Lombardi","year":"2019","journal-title":"Int J Mol Sci"},{"key":"pcbi.1008573.ref031","article-title":"Glycine-activated currents are changed by coincident membrane depolarization in developing rat auditory brainstem neurones","author":"KH Backus","year":"1998","journal-title":"J Physiol"},{"key":"pcbi.1008573.ref032","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fncel.2019.00497","article-title":"Coincident Activation of Glutamate Receptors Enhances GABAA Receptor-Induced Ionic Plasticity of the Intracellular Cl\u2212-Concentration in Dissociated Neuronal Cultures","volume":"13","author":"L Halbhuber","year":"2019","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref033","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1007932","article-title":"Chloride dynamics alter the input-output properties of neurons","volume":"16","author":"CB Currin","year":"2020","journal-title":"PLoS Comput Biol."},{"key":"pcbi.1008573.ref034","doi-asserted-by":"crossref","first-page":"2049","DOI":"10.1126\/science.1071111","article-title":"Correlated Bursts of Activity in the Neonatal Hippocampus in Vivo","volume":"296","author":"X Leinekugel","year":"2002","journal-title":"Science"},{"key":"pcbi.1008573.ref035","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/S0166-2236(00)01813-0","article-title":"Developing networks play a similar melody","volume":"24","author":"Y. Ben-Ari","year":"2001","journal-title":"Trends in Neurosciences"},{"key":"pcbi.1008573.ref036","doi-asserted-by":"crossref","first-page":"40","DOI":"10.3389\/fncir.2016.00040","article-title":"Spontaneous Neuronal Activity in Developing Neocortical Networks: From Single Cells to Large-Scale Interactions","volume":"10","author":"HJ Luhmann","year":"2016","journal-title":"Front Neural Circuits"},{"key":"pcbi.1008573.ref037","doi-asserted-by":"crossref","first-page":"12635","DOI":"10.1523\/JNEUROSCI.1922-15.2015","article-title":"Dynamic Changes from Depolarizing to Hyperpolarizing GABAergic Actions during Giant Depolarizing Potentials in the Neonatal Rat Hippocampus","volume":"35","author":"I Khalilov","year":"2015","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref038","doi-asserted-by":"crossref","first-page":"10398","DOI":"10.1523\/JNEUROSCI.3906-16.2017","article-title":"Interneuronal network activity at the onset of seizure-like events in entorhinal cortex slices","volume":"37","author":"L Librizzi","year":"2017","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref039","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1007\/s10827-012-0434-4","article-title":"A fast model of voltage-dependent NMDA receptors","volume":"34","author":"K Moradi","year":"2013","journal-title":"J Comput Neurosci"},{"key":"pcbi.1008573.ref040","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.tins.2007.03.012","article-title":"NMDA and AMPA receptors: old channels, new tricks","volume":"30","author":"VR Rao","year":"2007","journal-title":"Trends Neurosci"},{"key":"pcbi.1008573.ref041","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1152\/jn.1995.73.3.1157","article-title":"Computer simulations of morphologically reconstructed CA3 hippocampal neurons","volume":"73","author":"M Migliore","year":"1995","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref042","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/j.tins.2004.07.002","article-title":"Diversity of inhibitory neurotransmission through GABA(A) receptors","volume":"27","author":"I Mody","year":"2004","journal-title":"Trends Neurosci"},{"key":"pcbi.1008573.ref043","first-page":"18399","article-title":"NKCC-1 mediated Cl\u2212 uptake in immature CA3 pyramidal neurons is sufficient to compensate phasic GABAergic inputs","volume":"10","author":"SN Kolbaev","year":"2020","journal-title":"Sci Reports"},{"key":"pcbi.1008573.ref044","doi-asserted-by":"crossref","first-page":"255","DOI":"10.3389\/fncel.2017.00255","article-title":"Early Correlated Network Activity in the Hippocampus: Its Putative Role in Shaping Neuronal Circuits","volume":"11","author":"M Griguoli","year":"2017","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref045","first-page":"1","article-title":"Mild KCC2 Hypofunction Causes Inconspicuous Chloride Dysregulation that Degrades Neural Coding","volume":"9","author":"N Doyon","year":"2016"},{"key":"pcbi.1008573.ref046","doi-asserted-by":"crossref","first-page":"e1007661","DOI":"10.1371\/journal.pcbi.1007661","article-title":"An electrodiffusive, ion conserving Pinsky-Rinzel model with homeostatic mechanisms","volume":"16","author":"MJ S\u00e6tra","year":"2020","journal-title":"PLoS Computational Biology."},{"issue":"371","key":"pcbi.1008573.ref047","first-page":"1","article-title":"Development and regulation of chloride homeostasis in the central nervous system","volume":"9","author":"M Watanabe","year":"2015","journal-title":"Frontiers in Cellular Neuroscience"},{"key":"pcbi.1008573.ref048","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1152\/jn.1986.56.1.1","article-title":"Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons","volume":"56","author":"JR Huguenard","year":"1986","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref049","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1111\/j.1469-7793.1999.0693n.x","article-title":"Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl- and HCO3- transport","volume":"519","author":"KJ Staley","year":"1999","journal-title":"J Physiol"},{"key":"pcbi.1008573.ref050","doi-asserted-by":"crossref","first-page":"2034","DOI":"10.1152\/jn.00699.2010","article-title":"Effect of depolarizing GABA A-mediated membrane responses on excitability of cajal-retzius cells in the immature rat neocortex","volume":"106","author":"SN Kolbaev","year":"2011","journal-title":"J Neurophysiol"},{"key":"pcbi.1008573.ref051","doi-asserted-by":"crossref","first-page":"13016","DOI":"10.1523\/JNEUROSCI.1659-10.2010","article-title":"GABAergic synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential","volume":"30","author":"C Gonzalez-Islas","year":"2010","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref052","first-page":"1","article-title":"Temporal coding at the immature depolarizing gabaergic synapse","volume":"4","author":"G Valeeva","year":"2010","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref053","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1016\/j.neuron.2016.02.030","article-title":"Chloride Regulation: A Dynamic Equilibrium Crucial for Synaptic Inhibition","volume":"89","author":"N Doyon","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1008573.ref054","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1038\/nrn3819","article-title":"Cation-chloride cotransporters in neuronal development, plasticity and disease","volume":"15","author":"K Kaila","year":"2014","journal-title":"Nat Rev Neurosci"},{"key":"pcbi.1008573.ref055","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1744-8069-2-32","article-title":"Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: Towards a biophysical basis for neuropathic pain","volume":"2","author":"SA Prescott","year":"2006","journal-title":"Mol Pain"},{"key":"pcbi.1008573.ref056","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0172-17.2017","article-title":"Altered Chloride Homeostasis Decreases the Action Potential Threshold and Increases Hyperexcitability in Hippocampal Neurons","volume":"4","author":"AT Sorensen","year":"2017","journal-title":"eneuro"},{"key":"pcbi.1008573.ref057","doi-asserted-by":"crossref","first-page":"4017","DOI":"10.1523\/JNEUROSCI.5139-11.2012","article-title":"Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain","volume":"32","author":"V Dzhala","year":"2012","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref058","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/j.neuron.2009.08.022","article-title":"Differences in Cortical versus Subcortical GABAergic Signaling: A Candidate Mechanism of Electroclinical Uncoupling of Neonatal Seizures","volume":"63","author":"J Glykys","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1008573.ref059","doi-asserted-by":"crossref","first-page":"7750","DOI":"10.1038\/ncomms8750","article-title":"GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo","volume":"6","author":"K Kirmse","year":"2015","journal-title":"Nat Commun"},{"key":"pcbi.1008573.ref060","doi-asserted-by":"crossref","first-page":"5961","DOI":"10.1523\/JNEUROSCI.3482-15.2016","article-title":"An Optogenetic Approach for Investigation of Excitatory and Inhibitory Network GABA Actions in Mice Expressing Channelrhodopsin-2 in GABAergic Neurons","volume":"36","author":"G Valeeva","year":"2016","journal-title":"J Neurosci"},{"key":"pcbi.1008573.ref061","doi-asserted-by":"crossref","first-page":"3173","DOI":"10.1016\/j.celrep.2019.02.061","article-title":"Somatostatin Interneurons Promote Neuronal Synchrony in the Neonatal Hippocampus","volume":"26","author":"T Flossmann","year":"2019","journal-title":"Cell Rep"},{"key":"pcbi.1008573.ref062","doi-asserted-by":"crossref","first-page":"20","DOI":"10.3389\/fncel.2013.00020","article-title":"Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro","volume":"7","author":"G Valeeva","year":"2013","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref063","first-page":"26","article-title":"Taurine activates GABAergic networks in the neocortex of immature mice","volume":"8","author":"BA Sava","year":"2014","journal-title":"Front Cell Neurosci"},{"key":"pcbi.1008573.ref064","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1523\/JNEUROSCI.3861-04.2005","article-title":"Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held","volume":"25","author":"M Koike-Tani","year":"2005","journal-title":"J 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