{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:52:54Z","timestamp":1760147574948,"version":"build-2065373602"},"reference-count":106,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,2,15]],"date-time":"2023-02-15T00:00:00Z","timestamp":1676419200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["ERC- Stg #680235","113225"],"award-info":[{"award-number":["ERC- Stg #680235","113225"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Vaillant Fund","award":["ERC- Stg #680235","113225"],"award-info":[{"award-number":["ERC- Stg #680235","113225"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Purkinje cells (PCs) are the principal cells of the cerebellar cortex and form a central element in the modular organization of the cerebellum. Differentiation of PCs based on gene expression profiles revealed two subpopulations with distinct connectivity, action potential firing and learning-induced activity changes. However, which basal cell physiological features underlie the differences between these subpopulations and to what extent they integrate input differentially remains largely unclear. Here, we investigate the cellular electrophysiological properties of PC subpopulation in adult and juvenile mice. We found that multiple fundamental cell physiological properties, including membrane resistance and various aspects of the action potential shape, differ between PCs from anterior and nodular lobules. Moreover, the two PC subpopulations also differed in the integration of negative and positive current steps as well as in size of the hyperpolarization-activated current. A comparative analysis in juvenile mice confirmed that most of these lobule-specific differences are already present at pre-weaning ages. Finally, we found that current integration in PCs is input history-dependent for both positive and negative currents, but this is not a distinctive feature between anterior and nodular PCs. Our results support the concept of a fundamental differentiation of PCs subpopulations in terms of cell physiological properties and current integration, yet reveals that history-dependent input processing is consistent across PC subtypes.<\/jats:p>","DOI":"10.3390\/cells12040623","type":"journal-article","created":{"date-parts":[[2023,2,15]],"date-time":"2023-02-15T03:37:24Z","timestamp":1676432244000},"page":"623","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Lobule-Related Action Potential Shape- and History-Dependent Current Integration in Purkinje Cells of Adult and Developing Mice"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3038-5023","authenticated-orcid":false,"given":"Gerrit C.","family":"Beekhof","sequence":"first","affiliation":[{"name":"Department of Neuroscience, Erasmus MC, 3015 AA Rotterdam, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2675-1393","authenticated-orcid":false,"given":"Martijn","family":"Schonewille","sequence":"additional","affiliation":[{"name":"Department of Neuroscience, Erasmus MC, 3015 AA Rotterdam, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1038\/nature10732","article-title":"Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei","volume":"481","author":"Person","year":"2012","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1038\/nrn2698","article-title":"Cerebellar cortical organization: A one-map hypothesis","volume":"10","author":"Apps","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1007\/s12311-010-0221-6","article-title":"Cerebellar zones: A personal history","volume":"10","author":"Voogd","year":"2011","journal-title":"Cerebellum"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/wdev.65","article-title":"Development of the cerebellum: From gene expression patterns to circuit maps","volume":"2","author":"White","year":"2013","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_5","first-page":"448","article-title":"The Mammalian Cerebellum: Its Lobes and Fissures","volume":"38","author":"Bradley","year":"1904","journal-title":"J. Anat. Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/j.conb.2005.10.008","article-title":"Time and tide in cerebellar memory formation","volume":"15","author":"Yeo","year":"2005","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"12769","DOI":"10.1523\/JNEUROSCI.0197-12.2012","article-title":"Zebrin-Immunopositive and-Immunonegative Stripe Pairs Represent Functional Units in the Pigeon Vestibulocerebellum","volume":"32","author":"Graham","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1002\/cne.10952","article-title":"Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei: An analysis of single olivocerebellar axonal morphology","volume":"470","author":"Sugihara","year":"2004","journal-title":"J. Comp. Neurol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1007\/s12311-010-0204-7","article-title":"Visuomotor Cerebellum in Human and Nonhuman Primates","volume":"11","author":"Voogd","year":"2012","journal-title":"Cerebellum"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"9411","DOI":"10.1523\/JNEUROSCI.0440-10.2010","article-title":"Functional Relations of Cerebellar Modules of the Cat","volume":"30","author":"Horn","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1146\/annurev.neuro.23.1.649","article-title":"Synaptic Plasticity and Memory: An Evaluation of the Hypothesis","volume":"23","author":"Martin","year":"2000","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1126\/science.272.5265.1126","article-title":"The Cerebellum: A Neuronal Learning Machine?","volume":"272","author":"Jennifer","year":"1996","journal-title":"Science"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"8920","DOI":"10.1523\/JNEUROSCI.6117-09.2010","article-title":"Electrophysiological Localization of Eyeblink-Related Microzones in Rabbit Cerebellar Cortex","volume":"30","author":"Mostofi","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2493","DOI":"10.1523\/JNEUROSCI.4202-06.2007","article-title":"Acquisition, Extinction, and Reacquisition of a Cerebellar Cortical Memory Trace","volume":"27","author":"Jirenhed","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1097\/00001756-199401000-00030","article-title":"Suppression of cerebellar Purkinje cells during conditioned responses in ferrets","volume":"5","author":"Hesslow","year":"1994","journal-title":"NeuroReport"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"5715","DOI":"10.1523\/JNEUROSCI.21-15-05715.2001","article-title":"Acquisition of Eyeblink Conditioning Is Critically Dependent on Normal Function in Cerebellar Cortical Lobule HVI","volume":"21","author":"Attwell","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1038\/nrn3886","article-title":"Redefining the cerebellar cortex as an assembly of non-uniform Purkinje cell microcircuits","volume":"16","author":"Cerminara","year":"2015","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1038\/s41586-021-03220-z","article-title":"A transcriptomic atlas of mouse cerebellar cortex comprehensively defines cell types","volume":"598","author":"Kozareva","year":"2021","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1002\/cne.902910405","article-title":"Zebrin II: A polypeptide antigen expressed selectively by purkinje cells reveals compartments in rat and fish cerebellum","volume":"291","author":"Brochu","year":"1990","journal-title":"J. Comp. Neurol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2081","DOI":"10.1242\/dev.120.8.2081","article-title":"The cloning of zebrin II reveals its identity with aldolase C","volume":"120","author":"Ahn","year":"1994","journal-title":"Development"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0304-3940(97)00802-1","article-title":"A search for primitive Purkinje cells: Zebrin II expression in sea lampreys (Petromyzon marinus)","volume":"237","author":"Lannoo","year":"1997","journal-title":"Neurosci. Lett."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jchemneu.2008.10.001","article-title":"Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase C\u03b24","volume":"37","author":"Iwaniuk","year":"2009","journal-title":"Journal of Chemical Neuroanatomy"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1159\/000452857","article-title":"Zebrin II Is Expressed in Sagittal Stripes in the Cerebellum of Dragon Lizards (Ctenophorus sp.)","volume":"88","author":"Wylie","year":"2016","journal-title":"Brain Behav. Evol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/S0079-6123(04)48022-4","article-title":"Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species","volume":"148","author":"Sillitoe","year":"2005","journal-title":"Prog. Brain Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1002\/jnr.24206","article-title":"Regional differences in Purkinje cell morphology in the cerebellar vermis of male mice","volume":"96","author":"Nedelescu","year":"2018","journal-title":"J. Neurosci. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e63668","DOI":"10.7554\/eLife.63668","article-title":"Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors","volume":"10","author":"Beekhof","year":"2021","journal-title":"eLife"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e02536","DOI":"10.7554\/eLife.02536","article-title":"Cerebellar modules operate at different frequencies","volume":"3","author":"Zhou","year":"2014","journal-title":"eLife"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Xiao, J., Cerminara, N.L., Kotsurovskyy, Y., Aoki, H., Burroughs, A., Wise, A.K., Luo, Y., Marshall, S.P., Sugihara, I., and Apps, R. (2014). Systematic regional variations in Purkinje cell spiking patterns. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0105633"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1038\/s41586-022-04711-3","article-title":"Transcriptomic mapping uncovers Purkinje neuron plasticity driving learning","volume":"605","author":"Chen","year":"2022","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1002\/cne.21889","article-title":"Projection of reconstructed single purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum","volume":"512","author":"Sugihara","year":"2009","journal-title":"J. Comp. Neurol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1113\/jphysiol.1994.sp020017","article-title":"Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat","volume":"474","author":"Garwicz","year":"1994","journal-title":"J. Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/s12311-010-0226-1","article-title":"Compartmentalization of the Deep Cerebellar Nuclei Based on Afferent Projections and Aldolase C Expression","volume":"10","author":"Sugihara","year":"2011","journal-title":"Cerebellum"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Beekhof, G.C., Gornati, S.V., Canto, C.B., Libster, A.M., Schonewille, M., De Zeeuw, C.I., and Hoebeek, F.E. (2021). Activity of Cerebellar Nuclei Neurons Correlates with ZebrinII Identity of Their Purkinje Cell Afferents. Cells, 10.","DOI":"10.3390\/cells10102686"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1111\/j.1460-9568.2008.06294.x","article-title":"Multiple cerebellar zones are involved in the control of individual muscles: A retrograde transneuronal tracing study with rabies virus in the rat","volume":"28","author":"Ruigrok","year":"2008","journal-title":"Eur. J. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1007\/s12311-010-0164-y","article-title":"Ins and outs of cerebellar modules","volume":"10","author":"Ruigrok","year":"2011","journal-title":"Cerebellum"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"8771","DOI":"10.1523\/JNEUROSCI.1961-04.2004","article-title":"Molecular, Topographic, and Functional Organization of the Cerebellar Cortex: A study with Combined Aldolase C and Olivocerebellar labeling","volume":"24","author":"Sugihara","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"9696","DOI":"10.1523\/JNEUROSCI.1579-07.2007","article-title":"Molecular, Topographic, and Functional Organization of the Cerebellar Nuclei: Analysis by Three-Dimensional Mapping of the Olivonuclear Projection and Aldolase C Labeling","volume":"27","author":"Sugihara","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1023\/B:NEUR.0000029645.72074.2b","article-title":"The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern","volume":"33","author":"Voogd","year":"2004","journal-title":"J. Neurocytol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1007\/s12311-011-0347-1","article-title":"Parasagittal Zones in the Cerebellar Cortex Differ in Excitability, Information Processing, and Synaptic Plasticity","volume":"11","author":"Ebner","year":"2012","journal-title":"Cerebellum"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1007\/s12311-018-0968-8","article-title":"Depressed by Learning\u2014Heterogeneity of the Plasticity Rules at Parallel Fiber Synapses onto Purkinje Cells","volume":"17","author":"Suvrathan","year":"2018","journal-title":"Cerebellum"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1016\/S0301-0082(03)00114-X","article-title":"Patterned Purkinje cell death in the cerebellum","volume":"70","author":"Sarna","year":"2003","journal-title":"Prog. Neurobiol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Os\u00f3rio, C., White, J.J., Lu, H., Beekhof, G.C., Fiocchi, F.R., Andriessen, C.A., Dijkhuizen, S., Post, L., and Schonewille, M. (2022). Pre-ataxic loss of intrinsic plasticity and motor learning in a mouse model of SCA1. Brain, awac422.","DOI":"10.1093\/brain\/awac422"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/j.neuron.2016.11.046","article-title":"Motor Learning Requires Purkinje Cell Synaptic Potentiation through Activation of AMPA-Receptor Subunit GluA3","volume":"93","author":"Zhou","year":"2017","journal-title":"Neuron"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/j.neuron.2018.06.028","article-title":"Sensorimotor Integration and Amplification of Reflexive Whisking by Well-Timed Spiking in the Cerebellar Corticonuclear Circuit","volume":"99","author":"Brown","year":"2018","journal-title":"Neuron"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5301","DOI":"10.1113\/JP274346","article-title":"Mechanisms underlying vestibulo-cerebellar motor learning in mice depend on movement direction","volume":"595","author":"Voges","year":"2017","journal-title":"J. Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1977","DOI":"10.1016\/j.celrep.2015.10.057","article-title":"Evolving Models of Pavlovian Conditioning: Cerebellar Cortical Dynamics in Awake Behaving Mice","volume":"13","author":"Boele","year":"2015","journal-title":"Cell Rep."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1016\/j.neuron.2019.05.022","article-title":"Cerebellar Contribution to Preparatory Activity in Motor Neocortex","volume":"103","author":"Chabrol","year":"2019","journal-title":"Neuron"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/s41583-020-00392-x","article-title":"Bidirectional learning in upbound and downbound microzones of the cerebellum","volume":"22","year":"2021","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"13722","DOI":"10.1038\/ncomms13722","article-title":"Dendritic excitation\u2013inhibition balance shapes cerebellar output during motor behaviour","volume":"7","author":"Jelitai","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_50","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":"Mittmann","year":"2005","journal-title":"J. Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/nn1648","article-title":"Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia","volume":"9","author":"Walter","year":"2006","journal-title":"Nat. Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.neuron.2017.05.021","article-title":"Toward a Neurocentric View of Learning","volume":"95","author":"Titley","year":"2017","journal-title":"Neuron"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1523\/JNEUROSCI.19-05-01663.1999","article-title":"Ionic Currents Underlying Spontaneous Action Potentials in Isolated Cerebellar Purkinje Neurons","volume":"19","author":"Raman","year":"1999","journal-title":"J. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e45590","DOI":"10.7554\/eLife.45590","article-title":"TRPC3 is a major contributor to functional heterogeneity of cerebellar Purkinje cells","volume":"8","author":"Wu","year":"2019","journal-title":"eLife"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Grasselli, G., Boele, H.-J., Titley, H.K., Bradford, N., van Beers, L., Jay, L., Beekhof, G.C., Busch, S.E., De Zeeuw, C.I., and Schonewille, M. (2020). SK2 channels in cerebellar Purkinje cells contribute to excitability modulation in motor-learning\u2013specific memory traces. PLOS Biol., 18.","DOI":"10.1371\/journal.pbio.3000596"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.neuron.2012.05.025","article-title":"SK2 Channel Modulation Contributes to Compartment-Specific Dendritic Plasticity in Cerebellar Purkinje Cells","volume":"75","author":"Ohtsuki","year":"2012","journal-title":"Neuron"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.bbrc.2006.04.063","article-title":"The intrinsic mechanisms underlying the maturation of programming sequential spikes at cerebellar Purkinje cells","volume":"345","author":"Guan","year":"2006","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1113\/jphysiol.2001.013136","article-title":"Membrane potential bistability is controlled by the hyperpolarization-activated current I(H) in rat cerebellar Purkinje neurons in vitro","volume":"539","author":"Williams","year":"2002","journal-title":"J. Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"103705","DOI":"10.1016\/j.isci.2021.103705","article-title":"Heterogeneity of intrinsic plasticity in cerebellar Purkinje cells linked with cortical molecular zones","volume":"25","author":"Viet","year":"2022","journal-title":"iScience"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"152001","DOI":"10.1016\/j.acthis.2023.152001","article-title":"Calsequestrin in Purkinje cells of mammalian cerebellum","volume":"125","author":"Furlan","year":"2023","journal-title":"Acta Histochem."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Baroni, F., Torres, J.J., and Varona, P. (2011). History-Dependent Excitability as a Single-Cell Substrate of Transient Memory for Information Discrimination. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0015023"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"13481","DOI":"10.1073\/pnas.93.24.13481","article-title":"Memory from the dynamics of intrinsic membrane\u2009currents","volume":"93","author":"Marder","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.expneurol.2006.08.016","article-title":"Analysis of cerebellar Purkinje cells using EAAT4 glutamate transporter promoter reporter in mice generated via bacterial artificial chromosome-mediated transgenesis","volume":"203","author":"Gincel","year":"2007","journal-title":"Exp. Neurol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1038\/nature02033","article-title":"A gene expression atlas of the central nervous system based on bacterial artificial chromosomes","volume":"425","author":"Gong","year":"2003","journal-title":"Nature"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3606","DOI":"10.1523\/JNEUROSCI.18-10-03606.1998","article-title":"The Glutamate Transporter EAAT4 in Rat Cerebellar Purkinje Cells: A Glutamate-Gated Chloride Channel Concentrated near the Synapse in Parts of the Dendritic Membrane Facing Astroglia","volume":"18","author":"Dehnes","year":"1998","journal-title":"J. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Shin, S.L., Hoebeek, F.E., Schonewille, M., De Zeeuw, C.I., Aertsen, A., and De Schutter, E. (2007). Regular Patterns in Cerebellar Purkinje Cell Simple Spike Trains. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0000485"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1665","DOI":"10.1109\/TBME.2004.827531","article-title":"Estimating action potential thresholds from neuronal time-series: New metrics and evaluation of methodologies","volume":"51","author":"Sekerli","year":"2004","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1113\/jphysiol.2007.136465","article-title":"Propofol inhibits HCN1 pacemaker channels by selective association with the closed states of the membrane embedded channel core","volume":"583","author":"Lyashchenko","year":"2007","journal-title":"J. Physiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1007\/BF00585943","article-title":"Some properties of the UL-FS 49 block of the hyperpolarization-activated current (i(f)) in sino-atrial node myocytes","volume":"427","author":"DiFrancesco","year":"1994","journal-title":"Pflug. Arch."},{"key":"ref_70","first-page":"470","article-title":"HCN channels: Structure, cellular regulation and physiological function","volume":"66","author":"Biel","year":"2008","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2793","DOI":"10.1016\/S0024-3205(03)00182-6","article-title":"The anaesthetic agent propofol interacts with GABAB-receptors: An electrophysiological study in rat","volume":"72","author":"Schwieler","year":"2003","journal-title":"Life Sci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1038\/nrn3011","article-title":"Spatiotemporal firing patterns in the cerebellum","volume":"12","author":"Hoebeek","year":"2011","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"10603","DOI":"10.1523\/JNEUROSCI.22-24-10603.2002","article-title":"Active Contribution of Dendrites to the Tonic and Trimodal Patterns of Activity in Cerebellar Purkinje Neurons","volume":"22","author":"Womack","year":"2002","journal-title":"J. Neurosci."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1113\/jphysiol.1986.sp015993","article-title":"Inward rectification and low threshold calcium conductance in rat cerebellar Purkinje cells. An in vitro study","volume":"372","author":"Crepel","year":"1986","journal-title":"J. Physiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3389\/fncel.2012.00047","article-title":"The calcium-activated slow AHP: Cutting through the Gordian knot","volume":"6","author":"Andrade","year":"2012","journal-title":"Front. Cell. Neurosci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/S0092-8674(03)00884-5","article-title":"The Hyperpolarization-Activated HCN1 Channel Is Important for Motor Learning and Neuronal Integration by Cerebellar Purkinje Cells","volume":"115","author":"Nolan","year":"2003","journal-title":"Cell"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1007\/s12311-015-0724-2","article-title":"Consensus Paper: Cerebellar Development","volume":"15","author":"Leto","year":"2015","journal-title":"Cerebellum"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1038\/35081558","article-title":"Genetic regulation of cerebellar development","volume":"2","author":"Wang","year":"2001","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1152\/jn.00586.2014","article-title":"In vivo analysis of Purkinje cell firing properties during postnatal mouse development","volume":"113","author":"Arancillo","year":"2015","journal-title":"J. Neurophysiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1113\/jphysiol.2005.089383","article-title":"Physiological and morphological development of the rat cerebellar Purkinje cell","volume":"567","author":"McKay","year":"2005","journal-title":"J. Physiol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"2838","DOI":"10.1523\/JNEUROSCI.12-07-02838.1992","article-title":"Developmental changes in calcium conductances contribute to the physiological maturation of cerebellar Purkinje neurons in culture","volume":"12","author":"Gruol","year":"1992","journal-title":"J. Neurosci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1016\/j.bbrc.2016.08.141","article-title":"Expression and cellular localization of HCN channels in rat cerebellar granule neurons","volume":"478","author":"Valenzuela","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"5691","DOI":"10.1113\/jphysiol.2013.259499","article-title":"HCN1 channels in cerebellar Purkinje cells promote late stages of learning and constrain synaptic inhibition","volume":"591","author":"Rinaldi","year":"2013","journal-title":"J. Physiol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1038\/16697","article-title":"The K+\/Cl\u2212 co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation","volume":"397","author":"Rivera","year":"1999","journal-title":"Nature"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/cne.901710102","article-title":"Postnatal development of the cerebellar cortex in the rat: V. Spatial organization of Purkinje cell perikarya","volume":"171","author":"Altman","year":"1977","journal-title":"J. Comp. Neurol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.brainres.2006.05.001","article-title":"Developmental changes in the expression of GABAA receptor subunits \u03b11, \u03b12, and \u03b13 in brain stem nuclei of rats","volume":"1098","author":"Liu","year":"2006","journal-title":"Brain Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1002\/cne.10983","article-title":"Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride","volume":"468","author":"Stein","year":"2004","journal-title":"J. Comp. Neurol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"2161","DOI":"10.1152\/jn.00160.2009","article-title":"Membrane Capacitance Measurements Revisited: Dependence of Capacitance Value on Measurement Method in Nonisopotential Neurons","volume":"102","author":"Golowasch","year":"2009","journal-title":"J. Neurophysiol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Golowasch, J., and Nadim, F. (2013). Capacitance, Membrane. Encycl. Comput. Neurosci., 1\u20135.","DOI":"10.1007\/978-1-4614-7320-6_32-1"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"G3104","DOI":"10.1149\/2.0161812jes","article-title":"Identification of Capacitance Distribution in Neuronal Membranes from a Fractional-Order Electrical Circuit and Whole-Cell Patch-Clamped Cells","volume":"165","author":"Polo","year":"2018","journal-title":"J. Electrochem. Soc."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1016\/S0006-3495(00)76293-X","article-title":"Direct Measurement of Specific Membrane Capacitance in Neurons","volume":"79","author":"Gentet","year":"2000","journal-title":"Biophys. J."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1113\/jphysiol.1987.sp016517","article-title":"Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells","volume":"385","author":"Storm","year":"1987","journal-title":"J. Physiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainres.2008.03.030","article-title":"Iberiotoxin-sensitive large conductance Ca2+-dependent K+ (BK) channels regulate the spike configuration in the burst firing of cerebellar Purkinje neurons","volume":"1212","author":"Janahmadi","year":"2008","journal-title":"Brain Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"2528","DOI":"10.1152\/jn.00127.2012","article-title":"Iberiotoxin-sensitive and -insensitive BK currents in Purkinje neuron somata","volume":"109","author":"Mark","year":"2013","journal-title":"J. Neurophysiol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"2854","DOI":"10.1523\/JNEUROSCI.0192-20.2021","article-title":"BK Channel Regulation of Afterpotentials and Burst Firing in Cerebellar Purkinje Neurons","volume":"41","author":"Niday","year":"2021","journal-title":"J. Neurosci."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1038\/nrn2148","article-title":"The action potential in mammalian central neurons","volume":"8","author":"Bean","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/BF00583909","article-title":"Inward current activated during hyperpolarization in the rabbit sinoatrial node cell","volume":"385","author":"Yanagihara","year":"1980","journal-title":"Pfl\u00fcgers Arch."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"3339","DOI":"10.1152\/jn.00745.2015","article-title":"Corticotropin-releasing factor increases Purkinje neuron excitability by modulating sodium, potassium, and Ih currents","volume":"114","author":"Libster","year":"2015","journal-title":"J. Neurophysiol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"2446","DOI":"10.1152\/jn.00566.2015","article-title":"mGlu1 receptor mediates homeostatic control of intrinsic excitability through Ih in cerebellar Purkinje cells","volume":"115","author":"Shim","year":"2016","journal-title":"J. Neurophysiol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"513","DOI":"10.3389\/fncel.2018.00513","article-title":"Electrophysiological Excitability and Parallel Fiber Synaptic Properties of Zebrin-Positive and-Negative Purkinje Cells in Lobule VIII of the Mouse Cerebellar Slice","volume":"12","author":"Luo","year":"2019","journal-title":"Front. Cell. Neurosci."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Buchin, A., Rieubland, S., H\u00e4usser, M., Gutkin, B.S., and Roth, A. (2016). Inverse Stochastic Resonance in Cerebellar Purkinje Cells. PLOS Comput. Biol., 12.","DOI":"10.1371\/journal.pcbi.1005000"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1152\/jn.00369.2016","article-title":"Purkinje cell intrinsic excitability increases after synaptic long term depression","volume":"116","author":"Yang","year":"2016","journal-title":"J. Neurophysiol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"619747","DOI":"10.1155\/2012\/619747","article-title":"The Role of HCN Channels on Membrane Excitability in the Nervous System","volume":"2012","author":"Kase","year":"2012","journal-title":"J. Signal Transduct."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"e42766","DOI":"10.7554\/eLife.42766","article-title":"HCN channel-mediated neuromodulation can control action potential velocity and fidelity in central axons","volume":"8","author":"Byczkowicz","year":"2019","journal-title":"eLife"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1113\/jphysiol.2011.221846","article-title":"Lobule-specific membrane excitability of cerebellar Purkinje cells","volume":"590","author":"Kim","year":"2012","journal-title":"J. Physiol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.1038\/s42003-022-04283-y","article-title":"Postsynaptic plasticity of Purkinje cells in mice is determined by molecular identity","volume":"5","author":"Voerman","year":"2022","journal-title":"Commun. Biol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/4\/623\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:35:52Z","timestamp":1760121352000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/4\/623"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,15]]},"references-count":106,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["cells12040623"],"URL":"https:\/\/doi.org\/10.3390\/cells12040623","relation":{},"ISSN":["2073-4409"],"issn-type":[{"type":"electronic","value":"2073-4409"}],"subject":[],"published":{"date-parts":[[2023,2,15]]}}}