Journal Home > Volume 9 , Issue 1

Excitatory-inhibitory (E/I) balance is essential for normal neural development, behavior and cognition. E/I imbalance leads to a variety of neurological disorders, such as autism and schizophrenia. NMDA receptors (NMDARs) regulate AMPAR-mediated excitatory and GABAAR-mediated inhibitory synaptic transmission, suggesting that NMDARs play an important role in the establishment and maintenance of the E/I balance. In this review, we briefly introduced NMDARs, AMPARs and GABAARs, summarized the current studies on E/I balance mediated by NMDARs, and discussed the current advances in NMDAR-mediated AMPAR and GABAAR development. Specifically, we analyzed the role of NMDAR subunits in the establishment and maintenance of E/I balance, which may provide new therapeutic strategies for the recovery of E/I imbalance in neurological disorders.


menu
Abstract
Full text
Outline
About this article

NMDARs regulate the excitatory-inhibitory balance within neural circuits

Show Author's information Liang Zhou1( )Xiaohui Sun1Jingjing Duan2
College of Pharmaceutical Sciences, Soochow University, Suzhou 215123, Jiangsu, China
Department of Anatomy and Neurobiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China

Abstract

Excitatory-inhibitory (E/I) balance is essential for normal neural development, behavior and cognition. E/I imbalance leads to a variety of neurological disorders, such as autism and schizophrenia. NMDA receptors (NMDARs) regulate AMPAR-mediated excitatory and GABAAR-mediated inhibitory synaptic transmission, suggesting that NMDARs play an important role in the establishment and maintenance of the E/I balance. In this review, we briefly introduced NMDARs, AMPARs and GABAARs, summarized the current studies on E/I balance mediated by NMDARs, and discussed the current advances in NMDAR-mediated AMPAR and GABAAR development. Specifically, we analyzed the role of NMDAR subunits in the establishment and maintenance of E/I balance, which may provide new therapeutic strategies for the recovery of E/I imbalance in neurological disorders.

Keywords: NMDAR, AMPAR, GABAAR, excitatory-inhibitory balance, neurological disorders

References(115)

[1]
Levinson JN, El-Husseini A. Building excitatory and inhibitory synapses: balancing neuroligin partnerships. Neuron 2005, 48(2): 171–174.
[2]
Keck T, Scheuss V, Jacobsen RI, et al. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 2011, 71(5): 869–882.
[3]
Meechan DW, Tucker ES, Maynard TM, et al. Diminished dosage of 22q11 genes disrupts neurogenesis and cortical development in a mouse model of 22q11 deletion/DiGeorge syndrome. PNAS 2009, 106(38): 16434–16445.
[4]
Yizhar O, Fenno LE, Prigge M, et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011, 477(7363): 171–178.
[5]
Ben-Ari Y, Khazipov R, Leinekugel X, et al. GABAA, NMDA and AMPA receptors: a developmentally regulated ‘ménage à trois’. Trends Neurosci 1997, 20(11): 523–529.
[6]
Waites CL, Craig AM, Garner CC. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 2005, 28: 251–274.
[7]
Adesnik H, Li GN, During MJ, et al. NMDA receptors inhibit synapse unsilencing during brain development. Proc Natl Acad Sci USA 2008, 105(14): 5597–5602.
[8]
Lu W, Gray JA, Granger AJ, et al. Potentiation of synaptic AMPA receptors induced by the deletion of NMDA receptors requires the GluA2 subunit. J Neurophysiol 2011, 105(2): 923–928.
[9]
Marsden KC, Beattie JB, Friedenthal J, et al. NMDA receptor activation potentiates inhibitory transmission through GABA receptor-associated protein-dependent exocytosis of GABA(A) receptors. J Neurosci 2007, 27(52): 14326–14337.
[10]
Muir J, Arancibia-Carcamo IL, MacAskill AF, et al. NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the γ2 subunit. Proc Natl Acad Sci USA 2010, 107(38): 16679–16684.
[11]
Gu XL, Zhou L, Lu W. An NMDA receptor-dependent mechanism underlies inhibitory synapse development. Cell Rep 2016, 14(3): 471–478.
[12]
Tarabeux J, Kebir O, Gauthier J, et al. Rare mutations in N-methyl-D-aspartate glutamate receptors in autism spectrum disorders and schizophrenia. Transl Psychiatry 2011, 1(11): e55.
[13]
Liu SX, Zhou L, Yuan HJ, et al. A rare variant identified within the GluN2B C-Terminus in a patient with autism affects NMDA receptor surface expression and spine density. J Neurosci 2017, 37(15): 4093–4102.
[14]
Salpietro V, Dixon CL, Guo H, et al. AMPA receptor GluA2 subunit defects are a cause of neurodevelopmental disorders. Nat Commun 2019, 10(1): 3094.
[15]
Davies B, Brown LA, Cais O, et al. A point mutation in the ion conduction pore of AMPA receptor GRIA3 causes dramatically perturbed sleep patterns as well as intellectual disability. Hum Mol Genet 2017, 26(20): 3869–3882.
[16]
Charych EI, Liu F, Moss SJ, et al. GABA(A) receptors and their associated proteins: implications in the etiology and treatment of schizophrenia and related disorders. Neuropharmacology 2009, 57(5/6): 481–495.
[17]
Lorenz-Guertin JM, Bambino MJ, Jacob TC. γ2 GABA A R trafficking and the consequences of human genetic variation. Front Cell Neurosci 2018, 12: 265.
[18]
Zhang Z, Jiao YY, Sun QQ. Developmental maturation of excitation and inhibition balance in principal neurons across four layers of somatosensory cortex. Neuroscience 2011, 174: 10–25.
[19]
Paoletti P. Molecular basis of NMDA receptor functional diversity. Eur J Neurosci 2011, 33(8): 1351–1365.
[20]
Paoletti P, Bellone C, Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 2013, 14(6): 383–400.
[21]
Brothwell SLC, Barber JL, Monaghan DT, et al. NR2B- and NR2D-containing synaptic NMDA receptors in developing rat substantia nigra pars Compacta dopaminergic neurones. J Physiol 2008, 586(3): 739–750.
[22]
Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994, 17: 31–108.
[23]
Baez MV, Cercato MC, Jerusalinsky DA. NMDA receptor subunits change after synaptic plasticity induction and learning and memory acquisition. Neural Plast 2018, 2018: 5093048.
[24]
Lü W, Du J, Goehring A, et al. Cryo-EM structures of the triheteromeric NMDA receptor and its allosteric modulation. Science 2017, 355(6331): eaal3729.
[25]
Rajani V, Sengar AS, Salter MW. Tripartite signalling by NMDA receptors. Mol Brain 2020, 13(1): 23.
[26]
Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11(3): 327–335.
[27]
Chang HR, Kuo CC. The activation gate and gating mechanism of the NMDA receptor. J Neurosci 2008, 28(7): 1546–1556.
[28]
Benarroch EE. NMDA receptors: recent insights and clinical correlations. Neurology 2011, 76(20): 1750–1757.
[29]
Kehoe LA, Bernardinelli Y, Muller D. GluN3A: an NMDA receptor subunit with exquisite properties and functions. Neural Plast 2013, 2013: 145387.
[30]
Kuryatov A, Laube B, Betz H, et al. Mutational analysis of the Glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 1994, 12(6): 1291–1300.
[31]
Nowak L, Bregestovski P, Ascher P, et al. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984, 307(5950): 462–465.
[32]
Lau CG, Takeuchi K, Rodenas-Ruano A, et al. Regulation of NMDA receptor Ca2+ signalling and synaptic plasticity. Biochem Soc Trans 2009, 37(6): 1369–1374.
[33]
Guo HQ, Camargo LM, Yeboah F, et al. A NMDA-receptor calcium influx assay sensitive to stimulation by glutamate and glycine/D-serine. Sci Rep 2017, 7: 11608.
[34]
Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010, 11(10): 682–696.
[35]
Zhu SJ, Stein RA, Yoshioka C, et al. Mechanism of NMDA receptor inhibition and activation. Cell 2016, 165(3): 704–714.
[36]
Greger IH, Watson JF, Cull-Candy SG. Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins. Neuron 2017, 94(4): 713–730.
[37]
Henley JM, Wilkinson KA. Synaptic AMPA receptor composition in development, plasticity and disease. Nat Rev Neurosci 2016, 17(6): 337–350.
[38]
Lu W, Shi Y, Jackson AC, et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 2009, 62(2): 254–268.
[39]
Pickard L, Noël J, Henley JM, et al. Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci 2000, 20(21): 7922–7931.
[40]
Gründer T, Kohler K, Guenther E. Distribution and developmental regulation of AMPA receptor subunit proteins in rat retina. Invest Ophthalmol Vis Sci 2000, 41(11): 3600–3606.
[41]
Meador-Woodruff JH, Healy DJ. Glutamate receptor expression in schizophrenic brain. Brain Res Brain Res Rev 2000, 31(2/3): 288–294.
[42]
MacDonald RL, Olsen RW. GABAA receptor channels. Annu Rev Neurosci 1994, 17: 569–602.
[43]
Mody I, Pearce RA. Diversity of inhibitory neurotransmission through GABAA receptors. Trends Neurosci 2004, 27(9): 569–575.
[44]
Chang YC, Wang RP, Barot S, et al. Stoichiometry of a recombinant GABAAReceptor. J Neurosci 1996, 16(17): 5415–5424.
[45]
Tretter V, Ehya N, Fuchs K, et al. Stoichiometry and assembly of a recombinant GABAA receptor subtype. J Neurosci 1997, 17(8): 2728–2737.
[46]
Nguyen QA, Nicoll RA. The GABAA receptor β subunit is required for inhibitory transmission. Neuron 2018, 98(4): 718–725.e3.
[47]
Duan JJ, Pandey S, Li TM, et al. Genetic deletion of GABAA receptors reveals distinct requirements of neurotransmitter receptors for GABAergic and glutamatergic synapse development. Front Cell Neurosci 2019, 13: 217.
[48]
Laurie DJ, Wisden W, Seeburg PH. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 1992, 12(11): 4151–4172.
[49]
Jarrard LE. On the role of the Hippocampus in learning and memory in the rat. Behav Neural Biol 1993, 60(1): 9–26.
[50]
Paoletti P, Neyton J. NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 2007, 7(1): 39–47.
[51]
Bissen D, Foss F, Acker-Palmer A. AMPA receptors and their minions: auxiliary proteins in AMPA receptor trafficking. Cell Mol Life Sci 2019, 76(11): 2133–2169.
[52]
Olsen RW, Sieghart W. GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 2009, 56(1): 141–148.
[53]
Shu YS, Hasenstaub A, McCormick DA. Turning on and off recurrent balanced cortical activity. Nature 2003, 423(6937): 288–293.
[54]
Wehr M, Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426(6965): 442–446.
[55]
Turrigiano GG, Leslie KR, Desai NS, et al. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391(6670): 892–896.
[56]
He HY, Shen WH, Zheng LJ, et al. Excitatory synaptic dysfunction cell-autonomously decreases inhibitory inputs and disrupts structural and functional plasticity. Nat Commun 2018, 9(1): 2893.
[57]
He HY, Cline HT. What is excitation/inhibition and how is it regulated? A case of the elephant and the wisemen. J Exp Neurosci 2019, 13: 1179069519859371.
[58]
Sohal VS, Rubenstein JLR. Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders. Mol Psychiatry 2019, 24(9): 1248–1257.
[59]
Xue MS, Atallah BV, Scanziani M. Equalizing excitation–inhibition ratios across visual cortical neurons. Nature 2014, 511(7511): 596–600.
[60]
Shen WH, McKeown CR, Demas JA, et al. Inhibition to excitation ratio regulates visual system responses and behavior in vivo. J Neurophysiol 2011, 106(5): 2285–2302.
[61]
Nelson SB, Valakh V. Excitatory/inhibitory balance and circuit homeostasis in autism spectrum disorders. Neuron 2015, 87(4): 684–698.
[62]
Persson J. Wherefore ketamine? Curr Opin Anaesthesiol 2010, 23(4): 455–460.
[63]
Hirota K, Lambert DG. Ketamine: new uses for an old drug? Br J Anaesth 2011, 107(2): 123–126.
[64]
Bey T, Patel A. Phencyclidine intoxication and adverse effects: a clinical and pharmacological review of an illicit drug. Cal J Emerg Med 2007, 8(1): 9–14.
[65]
Su TH, Lu Y, Geng Y, et al. How could N-methyl-D-aspartate receptor antagonists lead to excitation instead of inhibition? Brain Sci Adv 2018, 4(2): 73–98.
[66]
Moghaddam B, Adams B, Verma A, et al. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 1997, 17(8): 2921–2927.
[67]
Gerhard DM, Pothula S, Liu RJ, et al. GABA interneurons are the cellular trigger for ketamine's rapid antidepressant actions. J Clin Investig 2020, 130(3): 1336–1349.
[68]
Miller OH, Yang LL, Wang CC, et al. GluN2B-containing NMDA receptors regulate depression-like behavior and are critical for the rapid antidepressant actions of ketamine. eLife 2014, 3: e03581.
[69]
Shepard R, Heslin K, Hagerdorn P, et al. Downregulation of Npas4 in parvalbumin interneurons and cognitive deficits after neonatal NMDA receptor blockade: relevance for schizophrenia. Transl Psychiatry 2019, 9(1): 99.
[70]
Spiegel I, Mardinly AR, Gabel HW, et al. Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 2014, 157(5): 1216–1229.
[71]
Chen XD, Shu SF, Bayliss DA. HCN1 channel subunits are a molecular substrate for hypnotic actions of ketamine. J Neurosci 2009, 29(3): 600–609.
[72]
Sleigh J, Harvey M, Voss L, et al. Ketamine - More mechanisms of action than just NMDA blockade. Trends Anaesth Crit Care 2014, 4(2/3): 76–81.
[73]
Zorumski CF, Izumi Y, Mennerick S. Ketamine: NMDA receptors and beyond. J Neurosci 2016, 36(44): 11158–11164.
[74]
Ferreira JS, Schmidt J, Rio P, et al. GluN2B-containing NMDA receptors regulate AMPA receptor traffic through anchoring of the synaptic proteasome. J Neurosci 2015, 35(22): 8462–8479.
[75]
Kehrer C, Maziashvili N, Dugladze T, et al. Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci 2008, 1: 6.
[76]
Gupta SC, Ravikrishnan A, Liu JX, et al. The NMDA receptor GluN2C subunit controls cortical excitatory-inhibitory balance, neuronal oscillations and cognitive function. Sci Rep 2016, 6: 38321.
[77]
Widman AJ, McMahon LL. Disinhibition of CA1 pyramidal cells by low-dose ketamine and other antagonists with rapid antidepressant efficacy. Proc Natl Acad Sci USA 2018, 115(13): E3007–E3016.
[78]
Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004, 44(1): 5–21.
[79]
Lüscher C, Malenka RC. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 2012, 4(6): a005710.
[80]
Diering GH, Huganir RL. The AMPA receptor code of synaptic plasticity. Neuron 2018, 100(2): 314–329.
[81]
Hall BJ, Ripley B, Ghosh A. NR2B signaling regulates the development of synaptic AMPA receptor current. J Neurosci 2007, 27(49): 13446–13456.
[82]
Ben-Yaacov A, Gillor M, Haham T, et al. Molecular mechanism of AMPA receptor modulation by TARP/stargazin. Neuron 2017, 93(5): 1126–1137.e4.
[83]
Zeng ML, Díaz-Alonso J, Ye F, et al. Phase separation-mediated TARP/MAGUK complex condensation and AMPA receptor synaptic transmission. Neuron 2019, 104(3): 529–543.e6.
[84]
Colledge M, Snyder EM, Crozier RA, et al. Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 2003, 40(3): 595–607.
[85]
Zhou L, Duan JJ. The C-terminus of NMDAR GluN1-1a subunit translocates to nucleus and regulates synaptic function. Front Cell Neurosci 2018, 12: 334.
[86]
Zhou L, Duan JJ. The NMDAR GluN1-1a C-terminus binds to CaM and regulates synaptic function. Biochem Biophys Res Commun 2021, 534: 323–329.
[87]
Marty S, Wehrlé R, Sotelo C. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 2000, 20(21): 8087–8095.
[88]
Mukherjee J, Kretschmannova K, Gouzer G, et al. The residence time of GABAARs at inhibitory synapses is determined by direct binding of the receptor 1 subunit to gephyrin. J Neurosci 2011, 31(41): 14677–14687.
[89]
Jacob TC, Bogdanov YD, Magnus C, et al. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci 2005, 25(45): 10469–10478.
[90]
Petrini EM, Ravasenga T, Hausrat TJ, et al. Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP. Nat Commun 2014, 5: 3921.
[91]
Lu W, Bromley-Coolidge S, Li J. Regulation of GABAergic synapse development by postsynaptic membrane proteins. Brain Res Bull 2017, 129: 30–42.
[92]
Horn ME, Nicoll RA. Somatostatin and parvalbumin inhibitory synapses onto hippocampal pyramidal neurons are regulated by distinct mechanisms. PNAS 2018, 115(3): 589–594.
[93]
Ben-Ari Y, Gaiarsa JL, Tyzio R, et al. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 2007, 87(4): 1215–1284.
[94]
Gundersen V, Talgøy Holten A, Storm-Mathisen J. GABAergic synapses in hippocampus exocytose aspartate on to NMDA receptors: quantitative immunogold evidence for co-transmission. Mol Cell Neurosci 2004, 26(1): 156–165.
[95]
LoTurco JJ, Blanton MG, Kriegstein AR. Initial expression and endogenous activation of NMDA channels in early neocortical development. J Neurosci 1991, 11(3): 792–799.
[96]
Demarque M. Glutamate transporters prevent the generation of seizures in the developing rat neocortex. J Neurosci 2004, 24(13): 3289–3294.
[97]
Lewerenz J, Maher P. Chronic glutamate toxicity in neurodegenerative diseases-What is the evidence? Front Neurosci 2015, 9: 469.
[98]
Gogolla N, Leblanc JJ, Quast KB, et al. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 2009, 1(2): 172–181.
[99]
Rylaarsdam L, Guemez-Gamboa A. Genetic causes and modifiers of autism spectrum disorder. Front Cell Neurosci 2019, 13: 385.
[100]
Hu C, Chen WJ, Myers SJ, et al. Human GRIN2B variants in neurodevelopmental disorders. J Pharmacol Sci 2016, 132(2): 115–121.
[101]
Yuan H, Low CM, Moody OA, et al. Ionotropic GABA and glutamate receptor mutations and human neurologic diseases. Mol Pharmacol 2015, 88(1): 203–217.
[102]
Yeganeh-Doost P, Gruber O, Falkai P, et al. The role of the cerebellum in schizophrenia: from cognition to molecular pathways. Clinics (Sao Paulo) 2011, 66(Suppl 1): 71–77.
[103]
Chen WJ, Shieh C, Swanger SA, et al. GRIN1 mutation associated with intellectual disability alters NMDA receptor trafficking and function. J Hum Genet 2017, 62(6): 589–597.
[104]
Lemke JR, Geider K, Helbig KL, et al. Delineating the GRIN1 phenotypic spectrum. Neurology 2016, 86(23): 2171–2178.
[105]
Ogden KK, Chen WJ, Swanger SA, et al. Molecular mechanism of disease-associated mutations in the pre-M1 helix of NMDA receptors and potential rescue pharmacology. PLoS Genet 2017, 13(1): e1006536.
[106]
Muhle R, Trentacoste SV, Rapin I. The genetics of autism. Pediatrics 2004, 113(5): e472–e486.
[107]
Numis AL, Major P, Montenegro MA, et al. Identification of risk factors for autism spectrum disorders in tuberous sclerosis complex. Neurology 2011, 76(11): 981–987.
[108]
Lozano R, Hare EB, Hagerman RJ. Modulation of the GABAergic pathway for the treatment of fragile X syndrome. Neuropsychiatr Dis Treat 2014, 10: 1769–1779.
[109]
Gao F, Qi LJ, Yang ZZ, et al. Impaired GABA neural circuits are critical for fragile X syndrome. Neural Plast 2018, 2018: 8423420.
[110]
Han S, Tai C, Westenbroek RE, et al. Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature 2012, 489(7416): 385–390.
[111]
Shin S, Santi A, Huang SY. Conditional Pten knockout in parvalbumin- or somatostatin-positive neurons sufficiently leads to autism-related behavioral phenotypes. Mol Brain 2021, 14(1): 24.
[112]
Saunders JA, Tatard-Leitman VM, Suh J, et al. Knockout of NMDA receptors in parvalbumin interneurons recreates autism-like phenotypes. Autism Res 2013, 6(2): 69–77.
[113]
Carlsson ML. Hypothesis: is infantile autism a hypoglutamatergic disorder? Relevance of glutamate - serotonin interactions for pharmacotherapy. J Neural Transm (Vienna) 1998, 105(4/5): 525–535.
[114]
Nabavi S, Kessels HW, Alfonso S, et al. Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. PNAS 2013, 110(10): 4027–4032.
[115]
Kessels HW, Nabavi S, Malinow R. Metabotropic NMDA receptor function is required for β-amyloid–induced synaptic depression. PNAS 2013, 110(10): 4033–4038.
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 18 May 2022
Revised: 20 June 2022
Accepted: 13 July 2022
Published: 27 February 2023
Issue date: March 2023

Copyright

© The authors 2023.

Acknowledgements

We thank Bullet Edits Limited for the linguistic editing and proofreading of the manuscript.

Rights and permissions

This article is published with open access at journals.sagepub.com/home/BSA

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).

Return