Evaluation of in vitro neuronal networks for the study of spontaneous activity

  • Diletta Pozzi Department of Otolaryngology, Head and Neck Surgery, Stanford University School of Medicine, USA
Keywords: Cortical oscillations, Up states, Calcium transients, Neuronal cultures, Brain slices

Abstract

In the absence of external stimuli, the nervous system exhibits a spontaneous electrical activity whose functions are not fully understood, and that represents the background noise of brain operations. Spontaneous activity has been proven to arise not only in vivo, but in in vitro neuronal networks as well, following some stereotypical patterns that reproduce the time course of development of the mammalian nervous system. This review provides an overview of in vitro models for the study of spontaneous network activity, discussing their ability to reproduce in vivo - like dynamics and the main findings obtained with each particular model. While explanted brain slices are able to reproduce the neuronal oscillations typically observed in anaesthetized animals, dissociated cultures allow the use of patient-derived neurons and limit the number of animals used for sample preparation.

Downloads

Download data is not yet available.

References

Berger H. Über das Elektrenkephalogramm des Menschen. Archiv f. Psychiatrie. 1929;87:527–570.

Freeman WJ. W.G. Walter: The Living Brain. In: Palm G, Aertsen A, editors. Brain Theory. Springer Berlin Heidelberg; 1986. p. 237–8.

Steriade M, Dossi RC, Nuñez A. Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. J Neurosci. 1991 Oct;11(10):3200–17.

Steriade M, Nuñez A, Amzica F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 1993 Aug;13(8):3252–65.

Sirota A, Buzsáki G. Interaction between neocortical and hippocampal networks via slow oscillations. Thalamus Relat Syst. 2005 Dec;3(04):245.

Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci. 1996 Apr 1;16(7):2397–410.

Constantinople CM, Bruno RM. Effects and mechanisms of wakefulness on local cortical networks. Neuron. 2011 Mar;69(6):1061–8.

Seeman SC, Campagnola L, Davoudian PA, Hoggarth A, Hage TA, Bosma-Moody A, et al. Sparse recurrent excitatory connectivity in the microcircuit of the adult mouse and human cortex. eLife. 2018 Sep 26;7:e37349.

Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G. The sleep slow oscillation as a traveling wave. J Neurosci. 2004 Aug 4;24(31):6862–70.

Capone C, Rebollo B, Muñoz A, Illa X, Del Giudice P, Sanchez-Vives MV, et al. Slow waves in cortical slices: how spontaneous activity is shaped by laminar structure. Cereb Cortex. 2019 Jan 1;29(1):319-335.

Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007 Jan;10(1):100–7.

Buzsáki G. Theta Oscillations in the hippocampus. Neuron. 2002 Jan;33(3):325–40.

Mohajerani MH, Cherubini E. Role of giant depolarizing potentials in shaping synaptic currents in the developing hippocampus. Crit Rev Neurobiol. 2006;18(1–2):13–23.

Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol. 1989 Sep;416:303–25.

Somogyi P, Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol. 2005 Jan 1;562(Pt 1):9–26.

Teleńczuk B, Dehghani N, Le Van Quyen M, Cash SS, Halgren E, Hatsopoulos NG, et al. Local field potentials primarily reflect inhibitory neuron activity in human and monkey cortex. Sci Rep. 2017 Jan 11;7:40211.

Cossart R, Aronov D, Yuste R. Attractor dynamics of network UP states in the neocortex. Nature. 2003 May 15;423(6937):283–8.

Thannickal TC1, Moore RY, Nienhuis R, Ramanathan L, Gulyani S, Aldrich M, Cornford M, Siegel JM. Reduced number of hypocretin neurons in human narcolepsy: Neuron. 2000 Sep;27(3):469-474.

Karbasforoushan H1, Woodward ND. Resting-state networks in schizophrenia. Curr Top Med Chem. 2012 Dec;12:2404-2414.

Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci. 1988 Apr;8(4):1454–68.

da Silva JS, Dotti CG. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci. 2002 Sep;3(9):694–704.

Eichberg J, Hauser G. The subcellular distribution of polyphosphoinositides in myelinated and unmyelinated rat brain. Biochim Biophys Acta BBA - Lipids Lipid Metab. 1973 Nov 29;326(2):210–23.

Hughes CS, Postovit LM, Lajoie GA. Matrigel: a complexprotein mixture required for optimal growth of cell culture. Proteomics. 2010 May;10(9):1886–90.

Pozzi D, Ban J, Iseppon F, Torre V. An improved method for growing neurons: comparison with standard protocols.J Neurosci Methods. 2017 Mar 15;280:1-10.

Lafon-Cazal M, Adjali O, Galeotti N, Poncet J, Jouin P, Homburger V, et al. Proteomic analysis of astrocytic secretion in the mouse: comparison with the cerebrospinal fluid proteome. J Biol Chem. 2003 Jun 27;278(27):24438–48.

Landis DM, Weinstein LA, Skordeles CJ. Serum influences the differentiation of membrane structure in cultured astrocytes. Glia. 1990;3(3):212–21.

Brewer GJ, Torricelli JR, Evege EK, Price PJ. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res. 1993 Aug 1;35(5):567–76.

Ivenshitz M, Segal M. Neuronal density determines network connectivity and spontaneous activity in cultured hippocampus. J Neurophysiol. 2010 Aug;104(2):1052–60.

Ebrahimi M, Yamamoto Y, Sharifi K, Kida H, Kagawa Y, Yasumoto Y, et al. Astrocyte-expressed FABP7 regulates dendritic morphology and excitatory synaptic function of cortical neurons. Glia. 2016 Jan;64(1):48–62.

Todd GK, Boosalis CA, Burzycki AA, Steinman MQ, Hester LD, Shuster PW, et al. Towards neuronal organoids: a method for long-term culturing of high-density hippocampal neurons. PloS One. 2013;8(4):e58996.

Weir K, Blanquie O, Kilb W, Luhmann HJ, Sinning A. Comparison of spike parameters from optically identified GABAergic and glutamatergic neurons in sparse cortical cultures. Front Cell Neurosci. 2014;8:460.

Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol. 2003 Dec 1;467(1):60–79.

Murphy TH, Blatter LA, Wier WG, Baraban JM. Spontaneous synchronous synaptic calcium transients in cultured cortical neurons. J Neurosci. 1992 Dec;12(12):4834–45.

Cohen E, Ivenshitz M, Amor-Baroukh V, Greenberger V, Segal M. Determinants of spontaneous activity in networks of cultured hippocampus. Brain Res. 2008 Oct 15;1235:21–30.

Björklund U, Persson M, Rönnbäck L, Hansson E. Primary cultures from cerebral cortex and hippocampus enriched in glutamatergic and GABAergic neurons. Neurochem Res. 2010 Nov;35(11):1733–42.

Biffi E, Regalia G, Menegon A, Ferrigno G, Pedrocchi A. The influence of neuronal density and maturation on network activity of hippocampal cell cultures: a methodological study. PLoS ONE. 2013 Dec 27;8(12):e83899.

Golshani P, Gonçalves JT, Khoshkhoo S, Mostany R, Smirnakis S, Portera-Cailliau C. Internally mediated developmental desynchronization of neocortical network activity. J Neurosci. 2009 Sep 2;29(35):10890–9.

Belle AM, Enright HA, Sales AP, Kulp K, Osburn J, Kuhn EA, et al. Evaluation of in vitro neuronal platforms as surrogates for in vivo whole brain systems. Sci Rep. 2018 Jul 17;8:10820.

Moskalyuk A, Kooy RF, Giugliano M. Single-cell and neuronal network alterations in an in vitro model of Fragile X syndrome. bioRxiv. 2018 Jul 10;366997.

Gonçalves JT, Anstey JE, Golshani P, Portera-Cailliau C. Circuit level defects in the developing neocortex of Fragile X mice. Nat Neurosci. 2013 Jul;16(7):903–9.

Testa-Silva G, Loebel A, Giugliano M, de Kock CPJ, Mansvelder HD, Meredith RM. Hyperconnectivity and slow synapses during early development of medial prefrontal cortex in a mouse model for mental retardation and autism. Cereb Cortex N Y N 1991. 2012 Jun;22(6):1333–42.

Prè D, Nestor MW, Sproul AA, Jacob S, Koppensteiner P, Chinchalongporn V, et al. A time course analysis of the electrophysiological properties of neurons differentiated from human induced pluripotent stem cells (iPSCs). PloS One. 2014;9(7):e103418.

Zhou R, Jiang G, Tian X, Wang X. Progress in the molecular mechanisms of genetic epilepsies using patient-induced pluripotent stem cells. Epilepsia Open. 2018 Jul 8;3(3):331–9.

Marton RM, Miura Y, Sloan SA, Li Q, Revah O, Levy RJ, et al. Differentiation and maturation of oligodendrocytes in human three-dimensional neural cultures. Nat Neurosci. 2019 Mar;22(3):484–91.

Irons HR, Cullen DK, Shapiro NP, Lambert NA, Lee RH, Laplaca MC. Three-dimensional neural constructs: a novel platform for neurophysiological investigation. J Neural Eng. 2008 Sep;5(3):333–41.

Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix Elasticity Directs Stem Cell Lineage Specification. Cell. 2006 Aug 25;126(4):677–89.

Lovat V, Pantarotto D, Lagostena L, Cacciari B, Grandolfo M, Righi M, et al. Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett. 2005 Jun;5(6):1107–10.

Cellot G, Toma FM, Varley ZK, Laishram J, Villari A, Quintana M, et al. Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial-tissue interactions. J Neurosci. 2011 Sep 7;31(36):12945–53.

Li N, Zhang Q, Gao S, Song Q, Huang R, Wang L, et al. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci Rep. 2013;3:1604.

Posypanova GA, Gayduchenko IA, Moskaleva EY, Fedorov GE. Neuronal differentiation of PC12 cells and mouse neural stem cells on carbon nanotube films. Cell Tissue Biol. 2016 May 1;10(3):194–201.

Ulloa Severino FP, Ban J, Song Q, Tang M, Bianconi G, Cheng G, et al. The role of dimensionality in neuronal network dynamics. Sci Rep. 2016 Jul 11;6:29640.

Pampaloni NP, Lottner M, Giugliano M, Matruglio A, D’Amico F, Prato M, et al. Single-layer graphene modulates neuronal communication and augments membrane ion currents. Nat Nanotechnol. 2018;13(8):755–64.

Bosi S, Rauti R, Laishram J, Turco A, Lonardoni D, Nieus T, et al. From 2D to 3D: novel nanostructured scaffolds to investigate signalling in reconstructed neuronal networks. Sci Rep. 2015;5:9562.

Aurand ER, Usmani S, Medelin M, Scaini D, Bosi S, Rosselli FB, et al. Nanostructures to engineer 3D neural-interfaces: directing axonal navigation toward successful bridging of spinal segments. Adv Funct Mater. 28(12):1700550.

Musick KM, Rigosa J, Narasimhan S, Wurth S, Capogrosso M, Chew DJ, et al. Chronic multichannel neural recordings from soft regenerative microchannel electrodes during gait. Sci Rep. 2015 Sep 24;5:14363.

Park D-W, Ness JP, Brodnick SK, Esquibel C, Novello J, Atry F, et al. Electrical neural stimulation and simultaneous in vivo monitoring with transparent graphene electrode arrays implanted in GCaMP6f mice. ACS Nano. 2018 23;12(1):148–57.

Masvidal-Codina E, Illa X, Dasilva M, Calia AB, Dragojević T, Vidal-Rosas EE, et al. High-resolution mapping of infraslow cortical brain activity enabled by graphene microtransistors. Nat Mater. 2019 Mar;18(3):280–8.

Li S, Severino FPU, Ban J, Wang L, Pinato G, Torre V, et al. Improved neuron culture using scaffolds made of three-dimensional PDMS micro-lattices. Biomed Mater. 2018;13(3):034105.

Wei J, Shi J, Wang B, Tang Y, Tu X, Roy E, et al. Fabrication of adjacent micropillar arrays with different heights for cell studies. Microelectron Eng. 2016 Jun;158:22–5.

Nagayama K, Inoue T, Hamada Y, Matsumoto T. A novel patterned magnetic micropillar array substrate for analysis of cellular mechanical responses. J Biomech. 2017 Dec 8;65:194–202.

Migliorini E, Ban J, Grenci G, Andolfi L, Pozzato A, Tormen M, et al. Nanomechanics controls neuronal precursors adhesion and differentiation. Biotechnol Bioeng. 2013;110(8):2301–10.

Wei J, Pozzi D, Ulloa Severino FP, Torre V, Chen Y. Fabrication of PLGA nanofibers on PDMS micropillars for neuron culture studies. Microelectron Eng. 2017 May;175(C):67–72.

D’Aiuto L, Naciri J, Radio N, Tekur S, Clayton D, Apodaca G, et al. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science. 2009 Dec 4;326(5958):1419–24.

Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 2000 Oct;3(10):1027–34.

Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV. Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci. 2008 Dec 17;28(51):13828–44.

Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 1997 Oct;20(10):471–7.

Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991 Apr;37(2):173–82.

Magalhães DM, Pereira N, Rombo DM, Beltrão-Cavacas C, Sebastião AM, Valente CA. Ex vivo model of epilepsy in organotypic slices—a new tool for drug screening. J Neuroinflammation. 2018 Jul 11;15(1):203.

Allene C, Picardo MA, Becq H, Miyoshi G, Fishell G, Cossart R. Dynamic changes in Interneuron morphophysiological properties mark the maturation of hippocampal network activity. J Neurosci. 2012 May 9;32(19):6688–98.

Crépel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R. A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron. 2007 Apr 5;54(1):105–20.

Okamoto K, Ishikawa T, Abe R, Ishikawa D, Kobayashi C, Mizunuma M, et al. Ex vivo cultured neuronal networks emit in vivo-like spontaneous activity. J Physiol Sci. 2014 Nov;64(6):421–31.

Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. 1995 Nov 2;378(6552):75–8.

Galarreta M, Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature. 1999 Nov 4;402(6757):72–5.

Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CCH. Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron. 2010 Feb;65(3):422–35.

Wickham J, Brödjegård NG, Vighagen R, Pinborg LH, Bengzon J, Woldbye DPD, et al. Prolonged life of human acute hippocampal slices from temporal lobe epilepsy surgery. Sci Rep. 2018 Mar 7;8(1):1–13.

Qi X-R, Verwer RWH, Bao A-M, Balesar RA, Luchetti S, Zhou J-N, et al. Human brain slice culture: a useful tool to study brain disorders and potential therapeutic compounds. Neurosci Bull. 2019 Apr;35(2):244–52.

Published
2020-03-03
How to Cite
Pozzi, D. (2020). Evaluation of in vitro neuronal networks for the study of spontaneous activity. STEMedicine, 1(2), e35. https://doi.org/10.37175/stemedicine.v1i2.35
Section
Review articles