Postnatal development of electrophysiological and morphological properties in layer 2/3 and layer 5 pyramidal neurons in the mouse primary visual cortex.
[en] Eye-opening is a critical point for laminar maturation of pyramidal neurons (PNs) in primary visual cortex. Knowing both the intrinsic properties and morphology of PNs from the visual cortex during development is crucial to contextualize the integration of visual inputs at different age stages. Few studies have reported changes in intrinsic excitability in these neurons but were restricted to only one layer or one stage of cortical development. Here, we used in vitro whole-cell patch-clamp to investigate the developmental impact on electrophysiological properties of layer 2/3 and layer 5 PNs in mouse visual cortex. Additionally, we evaluated the morphological changes before and after eye-opening and compared these in adult mice. Overall, we found a decrease in intrinsic excitability in both layers after eye-opening which remained stable between juvenile and adult mice. The basal dendritic length increased in layer 5 neurons, whereas spine density increased in layer 2/3 neurons after eye-opening. These data show increased number of synapses after onset of sensory input paralleled with a reduced excitability, presumably as homeostatic mechanism. Altogether, we provide a database of the properties of PNs in mouse visual cortex by considering the layer- and time-specific changes of these neurons during sensory development.
Research Center/Unit :
Systems Neurophysiology, Institute of Zoology, RWTH Aachen University
Ciganok-Hückels, Natalja ✱; Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany ; Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, 52074 Aachen, Germany
Jehasse, Kevin ✱; Université de Liège - ULiège > Département d'électricité, électronique et informatique (Institut Montefiore) > Systèmes et modélisation
Kricsfalussy-Hrabár, Lena; Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany
Ritter, Mira; Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany
Rüland, Thomas; Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany ; Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, 52074 Aachen, Germany ; Institute for Biological Information Processing (IBI-1), Forschungszentrum Jülich, 52428 Jülich, Germany
Kampa, Björn M ; Systems Neurophysiology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany ; Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, 52074 Aachen, Germany ; JARA BRAIN, Institute of Neuroscience and Medicine (INM-10), Forschungszentrum Jülich, 52428 Jülich, Germany
✱ These authors have contributed equally to this work.
Language :
English
Title :
Postnatal development of electrophysiological and morphological properties in layer 2/3 and layer 5 pyramidal neurons in the mouse primary visual cortex.
Baker A, Kalmbach B, Morishima M, Kim J, Juavinett A, Li N, Dembrow N. Specialized subpopulations of deep-layer pyramidal neurons in the neocortex: bridging cellular properties to functional consequences. J Neurosci. 2018:38(24):5441–5455.
Brown SP, Hestrin S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature. 2009:457(7233): 1133–1136.
Brown APY, Cossell L, Margrie TW. Visual experience regulates the intrinsic excitability of visual cortical neurons to maintain sensory function. Cell Rep. 2019:27(3):685–689.e4.
Davis GW, Bezprozvanny I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol. 2003:63:847–869.
De Roo M, Klauser P, Mendez P, Poglia L, Muller D. Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb Cortex. 2008:18(1):151–161.
Desai NS, Cudmore RH, Nelson SB, Turrigiano GG. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci. 2002:5(8):783–789.
Drager UC. Observations on monocular deprivation in mice. J Neurophysiol. 1978:41(1):28–42.
Espinosa JS, Stryker MP. Development and plasticity of the primary visual cortex. Neuron. 2012:75(2):230–249.
Etherington SJ, Williams SR. Postnatal development of intrinsic and synaptic properties transforms Signaling in the layer 5 excitatory neural network of the visual cortex. J Neurosci. 2011:31(26): 9526–9537.
Franceschetti S, Sancini G, Panzica F, Radici C, Avanzini G. Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex. Neuroscience. 1998:83(4):1013–1024.
FrankCA. How voltage-gated calcium channels gate forms of homeostatic synaptic plasticity. Front Cell Neurosci. 2014:8(40):1–14.
Frick A, Feldmeyer D, Sakmann B. Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex. J Physiol. 2007:585(1):103–116.
Goel A, Lee HK. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J Neurosci. 2007:27(25):6692–6700.
Gordon JA, Sttyker MP, Program NG, Keck WM. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci. 1996:16(10):3274–3286.
Gouwens NW, Sorensen SA, Berg J, Lee C, Jarsky T, Ting J, Sunkin SM, Feng D, Anastassiou CA, Barkan E, et al. Classification of electrophysiological and morphological neuron types in the mouse visual cortex. Nat Neurosci. 2019:22(7):1182–1195.
Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature. 2002:420(6917):812–816.
Gutzmann A, Ergül N, Grossmann R, Schultz C, Wahle P, Engelhardt M. A period of structural plasticity at the axon initial segment in developing visual cortex. Front Neuroanat. 2014:8(11):1–13.
Hoy JL, Niell CM. Layer-specific refinement of visual cortex function after eye opening in the awake mouse. J Neurosci. 2015:35(8): 3370–3383.
Jamann N, Dannehl D, Lehmann N, Wagener R, Thielemann C, Schultz C, Staiger J, Kole MHP, Engelhardt M. Sensory input drives rapid homeostatic scaling of the axon initial segment in mouse barrel cortex. Nat Commun. 2021:12(1):1–14.
Kim EJ, Juavinett AL, Kyubwa EM, Jacobs MW, Callaway EM. Three types of cortical layer 5 neurons that differ in brain-wide connectivity and function. Neuron. 2015:88(6):1253–1267.
Kroon T, van Hugte E, van Linge L, Mansvelder HD, Meredith RM. Early postnatal development of pyramidal neurons across layers of the mouse medial prefrontal cortex. Sci Rep. 2019:9(1):1–16.
Lendvai B, Stern EA, Chen B, Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature. 2000:404(6780):876–881.
Lom B, Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J Neurosci. 1999:19(22):9928–9938.
Lu W, Constantine-Paton M. Eye opening rapidly induces synaptic potentiation and refinement. Neuron. 2004:43(2):237–249.
Maffei A, Nelson SB, Turrigiano GG. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci. 2004:7(12):1353–1359.
Maffei A, Nataraj K, Nelson SB, Turrigiano GG. Potentiation of cortical inhibition by visual deprivation. Nature. 2006:443(7107):81–84.
Marx M, Feldmeyer D. Morphology and physiology of excitatory neurons in layer 6b of the somatosensory rat barrel cortex. Cereb Cortex. 2013:23(12):2803–2817.
Miller M. Maturation of rat visual cortex. I. a quantitative study of Golgi-impregnated pyramidal neurons. J Neurocytol. 1981:10(5): 859–878.
Niell CM. Cell types, circuits, and receptive fields in the mouse visual cortex. Annu Rev Neurosci. 2015:38(1):413–431.
Nuñez-Abades PA, He F, Barrionuevo G, Cameron WE. Morphology of developing rat genioglossal Motoneurons studied in vitro: changes in length, branching pattern, and spatial distribution of dendrites. J Comp Neurol. 1994:339:401420.
Oswald AMM, Reyes AD. Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J Neurophysiol. 2008:99(6):2998–3008.
Perez-García P, Pardillo-Díaz R, Geribaldi-Doldán N, Gómez-Oliva R, Domínguez-García S, Castro C, Nunez-Abades P, Carrascal L. Refinement of active and passive membrane properties of layer V pyramidal neurons in rat primary motor cortex during postnatal development. Front Mol Neurosci. 2021:14: 1–14.
Petit TL, Leboutillier JC, Gregorio A, Libstug H. The pattern of dendritic development in the cerebral cortex of the rat. Dev Brain Res. 1988:41(1-2):209–219.
Rátkai A, Tárnok K, Aouad HE, Micska B, Schlett K, Szücs A. Homeostatic plasticity and burst activity are mediated by hyperpolarization-activated cation currents and T-type calcium channels in neuronal cultures. Sci Rep. 2021:11(1):1–17.
Richards SEV, Moore AR, Nam AY, Saxena S, Paradis S, van Hooser SD. Experience-dependent development of dendritic arbors in mouse visual cortex. J Neurosci. 2020:40(34):6536–6556.
Rochefort NL, Garaschuk O, Milos R-I, Narushima M, Marandi N, Pichler B, Kovalchuk Y, Konnerth A. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc Natl Acad Sci U S A. 2009:106(35):15049–15054.
Romand S, Wang Y, Toledo-Rodriguez M, Markram H. Morphological development of thick-tufted layer V pyramidal cells in the rat somatosensory cortex. Front Neuroanat. 2011:5(5):1–27.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012:9(7):676–682.
Tatti R, Swanson OK, Lee MSE, Maffei A. Layer-specific developmental changes in excitation and inhibition in rat primary visual cortex. eNeuro. 2017:4(6):1–19.
Tien NW, Kerschensteiner D. Homeostatic plasticity in neural development. Neural Dev. 2018:13(1):1–7.
Turrigiano GG, Nelson SB. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci. 2004:5(2):97–107.
Turrigiano G, Abbott LF, Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science. 1994:264(5161): 974–977.
Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 1998:391(6670):892–896.
Van Aerde KI, Feldmeyer D. Morphological and physiological characterization of pyramidal neuron subtypes in rat medial prefrontal cortex. Cereb Cortex. 2015:25(3):788–805.
Virtanen MA, Lacoh CM, Fiumelli H, Kosel M, Tyagarajan S, de Roo M, Vutskits L. Development of inhibitory synaptic inputs on layer 2/3 pyramidal neurons in the rat medial prefrontal cortex. Brain Struct Funct. 2018:223(4):1999–2012.
Wallace W, Bear MF. A morphological correlate of synaptic scaling in visual cortex. J Neurosci. 2004:24(31):6928–6938.
Yoshii A, Sheng MH, Constantine-Paton M. Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc Natl Acad Sci U S A. 2003:100(3):1334–1339.
Zhang ZW. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol. 2004:91(3):1171–1182.
Zhao JP, Phillips MA, Constantine-Paton M. Long-term potentiation in the juvenile superior colliculus requires simultaneous activation of NMDA receptors and L-type Ca2+ channels and reflects addition of newly functional synapses. J Neurosci. 2006:26(49): 12647–12655.
