Throughout life, neural circuits change their connectivity, especially during development, when neurons frequently extend and retract dendrites and axons, and form and eliminate synapses. In spite of their changing connectivity, neural circuits maintain relatively constant activity levels. Neural circuits achieve functional stability by homeostatic plasticity, which equipoises intrinsic excitability and synaptic strength, balances network excitation and inhibition, and coordinates changes in circuit connectivity. Here, we review how diverse mechanisms of homeostatic plasticity stabilize activity in developing neural circuits. Keywords: Homeostatic plasticity, Neural development, Intrinsic excitability, Synaptic strength, Excitation/inhibition ratio, Patterned spontaneous activity Background Homeostatic regulation of intrinsic excitability Nervous systems face a constant challenge: how to Neuronal intrinsic excitability is determined by the density, maintain flexibility and stability at the same time. Neural distribution, and function of ion channels, and controls circuits must stay flexible to allow for changes in con- how synaptic inputs are converted into action potential out- nectivity and synaptic strength during development and puts . Several studies have found a reciprocal relationship learning. As changes in connectivity push neural circuits between intrinsic excitability and synaptic inputs across de- away from equilibrium, they need to maintain activity velopment, which stabilizes activity [10–12]. As synaptic in- within a working range and avoid extremes of quies- puts increase in developing Xenopus retinotectal circuits, cence and saturation. Functional stability is maintained Na currents decrease, reducing intrinsic excitability . by homeostatic plasticity, which is defined broadly as a Conversely, silencing synaptic inputs to developing Xenopus set of neuronal changes that restore activity to a setpoint tectal neurons and Drosophila motorneurons increases Na following perturbation [1–3]. Recent studies have identi- currents and intrinsic excitability [10, 12, 13]. Several fied diverse homeostatic plasticity mechanisms triggered mechanisms mediate homeostatic changes in Na currents. by a variety of perturbations. These mechanisms regulate Translational repression and post-translational phosphoryl- dendritic and axonal connectivity of a neuron, as well as ation reduce the density and open probability, respectively, its intrinsic excitability (Fig. 1). In addition to maintain- of voltage-gated Na channels in Drosophila motorneurons ing the activity of individual neurons, homeostatic plasti- and rat cortical neurons in response to elevated city can act at a network level to coordinate changes in synaptic activity [11, 14–17]. connectivity and excitability across multiple neurons to Multiple ion channels in the same neuron can balance stabilize circuit function  (Fig. 2). Several recent re- each other to stabilize activity [2, 18, 19]. For example, the views have covered the function of homeostatic plasticity A-type K channels shal and shaker are reciprocally in the mature nervous system [5–8]. Here, we focus on regulated in motorneurons of Drosophila larvae: shaker is homeostatic plasticity in developing circuits. up-regulated in shal mutants, and shal is up-regulated in shaker mutants . However, compensatory expression is not always a two-way street; in Drosophila mutants of the delayed rectifier K channel shab, increased expression of * Correspondence: email@example.com; firstname.lastname@example.org 2+ + 1 the Ca -dependent K channel slo prevents motorneuron Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, USA hyperactivity, but, loss of slo does not increase expression Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Tien and Kerschensteiner Neural Development (2018) 13:9 Page 2 of 7 Fig. 1 Diverse homeostatic plasticity mechanisms stabilize the activity of developing neurons. When the activity of individual neurons decreases below (1 and 2) or increases above (3 and 4) a setpoint, homeostatic regulation of synaptic strength (1 and 3) and/or intrinsic excitability (2 and 4) acts to restore normal activity. By increasing (1) or decreasing (3) synaptic input (e.g., changes in mEPSC amplitude or frequency), a neuron’soutput firing rate can be shifted up or down to the target activity (grey area). By increasing (2) or decreasing (4) intrinsic excitability (e.g., changes in the length and location of AIS), a neuron’s input/output relationship can be modified of shab . Neurons can synergistically regulate ion translation, post-translational modifications, and traf- channels with opposite effects on excitability to restore ficking, can alter intrinsic excitability and balance activity. Silencing of pyramidal neurons cultured from changes in synaptic input to maintain activity homeo- visual cortex of rat pups with TTX increases Na currents stasis [9, 34–36]. and decreases K currents . Finally, neurons of the same type with similar excitability can vary significantly in Homeostatic regulation of synapse strength and number their membrane conductances, which may reflect the Homeostatic plasticity can regulate synaptic strength complex homeostatic interactions between ion channels pre- and postsynaptically, and its dominant expression [23–25](formore discussion, see[26, 27]). site can shift during development. In the early stages of Detailed examination of the distribution of ion chan- network formation, miniature excitatory postsynaptic nels revealed an important role of the axon-initial- current (mEPSC) amplitudes increase when spike gener- segment (AIS) in intrinsic homeostatic plasticity. ation is blocked in cortical and hippocampal neuron cul- Changes in length and location of the AIS, a specialized tures (i.e., suppression of intrinsic excitability), indicative + + region with clusters of voltage-gated Na and K of postsynaptic changes in AMPA receptor accumulation channels involved in spike generation, can counter the . At later stages, presynaptic regulation of vesicle re- effects of sensory deprivation or photostimulation [28–31]. lease and recycling is added, and mEPSC frequencies In mice, eye opening at postnatal day 13–14 shortens increase along with mEPSC amplitudes when spike gener- the AIS of pyramidal neurons in visual cortex [32, 33]. ation is blocked [37, 38]. This suggests a developmental Together, adjustments in ion channel density, distribution, shift in the capacity for pre- and postsynaptic homeostatic and function, resulting from changes in transcription, plasticity . Homeostatic control of synaptic strength Tien and Kerschensteiner Neural Development (2018) 13:9 Page 3 of 7 Fig. 2 Network-level homeostatic plasticity stabilizes activity of developing circuits. Network activity homeostasis is achieved by balancing excitation (red) and inhibition (blue). Synaptic strength and connectivity can be regulated in a cell-type-specific manner to maintain network homeostasis. Upward/downward red arrows: increased/decreased excitatory drive; upward/downward blue arrows: increased/decreased inhibitory drive has also been observed in vivo [39, 40]. The extent and ex- which strengthen their connections [53, 54]. Thus, pre- pression site of this control depends on circuit maturation synaptic neurotransmitter release, postsynaptic receptor [41–45]. Homeostatic synaptic plasticity in layers 4 and 6 abundance, and synapse number are homeostatically co- of primary visual cortex elicited by visual deprivation is re- regulated during normal development and after activity stricted to an early critical period (postnatal day 16 to 21) perturbations. In several systems, the expression sites [42, 43]. Later, homeostatic regulation of mEPSC ampli- and the combination of mechanisms engaged shift tudes shifts to layers 2/3, where it persists into adulthood across development [2, 3, 55–57]. [42, 44]. The purpose of this shift in homeostatic plasticity across cortical layers remains unknown . Chronic ac- Homeostatic regulation of network activity tivity suppression by intracranial infusion of the Na Homeostatic plasticity can stabilize the activity of individ- channel blocker TTX or NMDA receptor blockers ual neurons [54, 58, 59]. Neurons connect to each other increases spine densities of developing thalamocortical in a cell-type-specific manner, forming circuits that per- neurons in the dorsolateral geniculate nucleus of cats and form specific functions. In the following sections, we dis- ferrets [46, 47]. Thus, homeostatic plasticity can regulate cuss how homeostatic mechanisms are coordinated across synapse number as well as strength [48–50]. neurons to stabilize circuit function [4, 60]. In addition to homeostatic synaptic changes elicited by experimental perturbations, Desai et al. showed that Homeostatic regulation of network excitation and inhibition across development, mEPSC amplitudes in layers 2/3 Network activity is determined by the ratio of excitation and 4 of rat primary visual cortex decrease as mEPSC and inhibition (E/I ratio) [1, 4, 61]. In response to per- frequencies and synapse numbers increase . Retino- turbations, developing circuits can differentially adjust geniculate circuits provide another example of develop- inhibitory and excitatory connectivity to alter the E/I ra- mental homeostatic co-regulation [51–53]. Initially, tio and restore activity [62–65]. In developing hippo- many retinal ganglion cells converge onto thalamocorti- campal and organotypic cerebellar cultures, TTX or cal cells, each forming weak connections. Then, for up glutamate receptor antagonists decrease inhibitory syn- to 3 weeks after eye opening, thalamocortical cells prune apse densities and strengths, whereas blocking GABAer- inputs, retaining synapses from fewer ganglion cells, gic transmission with bicuculline increases the density of Tien and Kerschensteiner Neural Development (2018) 13:9 Page 4 of 7 inhibitory synapses. Similarly, brain slice recordings in neurons, homeostatic plasticity may act in a cell-type- barrel cortex layer 4 showed that sensory deprivation specific manner to stabilize circuit function . In the selectively reduces inhibitory input to layer 4 spiny developing dentate gyrus, loss of excitatory drive by tet- neurons in young but not in adult animals [66, 67]. anus toxin expression results in reduced inhibitory input Activity-dependent changes in inhibitory synaptic to granule cells . This reduction is cell-type specific, transmission appear to be regulated non-cell autono- affecting somatic innervation by parvalbumin-positive mously, as activity suppression of individual presynap- basket cells, but not dendritic innervation by calretinin- tic or postsynaptic cells failed to elicit compensatory and somatostatin-expressing interneurons. Selective re- changes observed after global application of TTX in duction of somatic inhibition efficiently restores the neonatal cultured hippocampal neurons . It has firing of granule cells [82, 83]. Similarly, monocular been suggested that inhibitory interneurons may sacri- deprivation during a pre-critical period was shown to fice their own firing rate homeostasis to stabilize spik- regulate feedback but not feedforward inhibition to layer ing of cortical pyramidal neurons after global activity 4 pyramidal cells in rat primary visual cortex ; and blockade [4, 68]. Another example of network homeo- early hearing loss weakens inhibitory synapses from fast- stasis comes from studies of monocular deprivation spiking interneurons but not from low-threshold spiking during the critical period . Here, homeostatic plas- interneurons onto pyramidal cells [85, 86]. ticity adjusts recurrent and feedforward connections Homeostatic regulation of excitatory connectivity can between layer 4 circuits and layer 2/3 circuits in pri- also be cell type specific . In the developing mouse mary visual cortex. Visual deprivation via intraocular retina, following removal of their dominant B6 bipolar TTX injection increases the excitatory drive and reduces cell input, ONα retinal ganglion cells up-regulate con- inhibitory drive from layer 4 to layer 2/3, compensating nectivity with XBC, B7, and rod bipolar cells, but leave for the lost excitatory sensory input [4, 69, 70]. Intri- input from B8 bipolar cells unchanged. This cell-type- guingly, in another deprivation paradigm (i.e., lid suture), specific rewiring not only maintains the sustained ac- increased intrinsic excitability and decreased E/I ratios tivity of ONα retinal ganglion cells, but also precisely stabilize activity in layer 2/3, indicating the same circuit preserves their light responses. Thus, homeostatic can use different combinations of homeostatic mecha- plasticity can regulate inhibitory and excitatory connectiv- nisms to compensate for sensory deprivation. ity in a cell-type-specific manner to maintain the activity In addition to regulating excitatory and inhibitory syn- and sensory function of developing circuits. apse strength and number, homeostatic plasticity can switch the transmitter phenotype of neurons from glu- Homeostatic regulation of patterned spontaneous activity tamate to GABA or vice versa to adjust the E/I ratio of Throughout the nervous system, developing circuits developing circuits [71–73]. In the embryonic Xenopus spontaneously generate activity patterns that help refine spinal cord, the fractions of neurons expressing excita- their connectivity [88, 89]. Before eye opening, waves of tory transmitters increase and decrease, respectively, activity originating in the retina propagate through the when network activity is pharmacologically suppressed visual system and dominate activity up to primary visual and enhanced. These switches in transmitter phenotype cortex [90–92]. Retinal waves mature in three stages occur without changes in the expression of cell identity (I-III), in which different circuit mechanisms generate markers . Similar to homeostatic regulation of in- distinct activity patterns that serve specific functions hibitory synapses, the activity-dependent transmitter in visual system refinement . In mice, stage I switch is non-cell autonomous and depends on network waves, which are mediated by gap-junctional coupling activity, evidenced by the reciprocal relationship between of retinal ganglion cells, were first observed at embry- the number of silenced cells and the ratio of neurons ex- onic day 17. Around birth, the wave generation pressing GABA vs. glutamate . Whether switches in switches to networks of cholinergic amacrine cells transmitter phenotypes contribute to network homeosta- (stage II, postnatal day 1–10) followed in the second sis during normal development remains to be investi- postnatal week by glutamatergic input from bipolar gated . cells (stage III, postnatal day 10–14). The transitions between stages appear to be homeostatically regulated. Homeostatic regulation of cell-type-specific connectivity When stage II (i.e., cholinergic) waves are disrupted Recent advances in single-cell RNA sequencing together by genetic deletion or pharmacological blockade of ß2 with large-scale morphological and functional surveys nicotinic acetylcholine receptors nAChRs, stage I have revealed a great diversity of excitatory and inhibi- waves persist until premature stage III waves take tory cell types, which serve distinct circuit functions over [93–96]. Similarly, in VGluT1 knockout mice, in [76–79]. This raises the questions whether, beyond cat- which stage III waves are abolished, stage II waves egorical differences between excitatory and inhibitory persist until eye opening . Studies of developing Tien and Kerschensteiner Neural Development (2018) 13:9 Page 5 of 7 spinal networks revealed an important role of excita- Authors’ contributions N-WT and DK wrote the manuscript. Both authors read and approved the tory GABAergic currents in homeostatic regulation of final manuscript. patterned spontaneous activity . During develop- ment, GABA switches from excitatory to inhibitory as Ethics approval and consent to participate initially high intracellular Cl concentrations are lowered Not applicable. by the developmentally regulated expression of cation- chloride cotransporters [99, 100]. When spontaneous net- Competing interests The authors declare that they have no competing interests. work activity in chick embryos was reduced by injection of a sodium channel blocker, excitatory GABAergic mEPSC amplitudes were found to increase because of an Publisher’sNote − − Springer Nature remains neutral with regard to jurisdictional claims in increased Cl driving force due to intracellular Cl published maps and institutional affiliations. accumulation [101, 102]. Although homeostatic mechanisms can restore spontan- Author details Department of Ophthalmology and Visual Sciences, Washington University eous activity patterns following perturbations, the extent School of Medicine, Saint Louis, USA. Graduate Program in Neuroscience, to which these activity patterns support normal circuit re- Washington University School of Medicine, Saint Louis, USA. Department of finement varies depending on age and means of perturb- Neuroscience, Washington University School of Medicine, Saint Louis, USA. Department of Biomedical Engineering, Washington University School of ation and needs to be further investigated [103–105]. Medicine, Saint Louis, USA. Hope Center for Neurological Disorders, Washington University School of Medicine, Saint Louis, MO 63110, USA. Conclusions Received: 9 January 2018 Accepted: 24 April 2018 Developing circuits undergo profound changes in con- nectivity that threaten to destabilize their activity. Recent References research has revealed a diverse set of homeostatic plasti- 1. Turrigiano GG, Nelson SB. Homeostatic plasticity in the developing nervous city mechanisms, which safeguard activity of developing system. Nat Rev Neurosci. 2004;5(2):97–107. circuits. Different combinations of these mechanisms are 2. Davis GW. Homeostatic signaling and the stabilization of neural function. Neuron. 2013;80(3):718–28. recruited by different perturbations in different neuronal 3. Wefelmeyer W, Puhl CJ, Burrone J. Homeostatic plasticity of subcellular neuronal cell types at different stages of development. What sig- structures: from inputs to outputs. Trends Neurosci. 2016;39(10):656–67. nals control the recruitment of specific combinations of 4. Maffei A, Fontanini A. Network homeostasis: a matter of coordination. Curr Opin Neurobiol. 2009;19(2):168–73. mechanisms is unclear and an interesting topic for 5. Fox K, Stryker M. Integrating Hebbian and homeostatic plasticity: future studies [41, 55]. introduction. Philos Trans R Soc Lond Ser B Biol Sci. 2017;372(1715). https:// Another important and mostly unanswered question is doi.org/10.1098/rstb.2016.0413. 6. Turrigiano GG. The dialectic of Hebb and homeostasis. Philos Trans R Soc how activity setpoints are determined [2, 106–108]. Lond Ser B Biol Sci. 2017;372(1715). https://doi.org/10.1098/rstb.2016.0258. Recent evidence suggests that this may occur during 7. Turrigiano GG. The self-tuning neuron: synaptic scaling of excitatory synapses. specific critical periods of development [109, 110]. Alter- Cell. 2008;135(3):422–35. 8. Vitureira N, Goda Y. Cell biology in neuroscience: the interplay between ing network activity in wild-type Drosophila during a Hebbian and homeostatic synaptic plasticity. J Cell Biol. 2013;203(2):175–86. critical period induces subsequent seizures, whereas cor- 9. Beck H, Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. recting abnormal activity in mutant flies during the same Nat Rev Neurosci. 2008;9(5):357–69. 10. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M. Altered electrical period is sufficient to suppress seizures for life. Import- properties in Drosophila neurons developing without synaptic transmission. antly, in the seizure-prone flies, homeostatic plasticity J Neurosci. 2001;21(5):1523–31. mechanisms are intact, but working toward the “wrong” 11. Baines RA. Postsynaptic protein kinase a reduces neuronal excitability in response to increased synaptic excitation in the Drosophila CNS. J Neurosci. setpoints. Insights into critical period timing and deter- 2003;23(25):8664–72. minants of activity setpoints could have significant im- 12. Pratt KG, Aizenman CD. Homeostatic regulation of intrinsic excitability and plications for the treatment of neurodevelopmental synaptic transmission in a developing visual circuit. J Neurosci. 2007;27(31): 8268–77. diseases including epilepsy and autisms [111–114]. 13. Hamodi AS, Pratt KG. Region-specific regulation of voltage-gated intrinsic currents in the developing optic tectum of the Xenopus tadpole. J Neurophysiol. 2014;112(7):1644–55. Abbreviations 14. Mee CJ, Pym EC, Moffat KG, Baines RA. Regulation of neuronal excitability AIS: Axon-initial-segment; E/I: Excitation/Inhibition; mEPSC: miniature excitatory through pumilio-dependent control of a sodium channel gene. J Neurosci. postsynaptic current 2004;24(40):8695–703. 15. Muraro NI, Weston AJ, Gerber AP, Luschnig S, Moffat KG, Baines RA. Pumilio binds Para mRNA and requires Nanos and brat to regulate sodium current Funding in Drosophila motoneurons. J Neurosci. 2008;28(9):2099–109. Work of the authors was supported by funding from the National Institutes 16. Driscoll HE, Muraro NI, He M, Baines RA. Pumilio-2 regulates translation of of Health (NIH EY023441, EY026978, and EY027411). Nav1.6 to mediate homeostasis of membrane excitability. J Neurosci. 2013; 33(23):9644–54. Availability of data and materials 17. Scheuer T. Regulation of sodium channel activity by phosphorylation. Semin Data sharing not applicable to this review article. Cell Dev Biol. 2011;22(2):160–5. Tien and Kerschensteiner Neural Development (2018) 13:9 Page 6 of 7 18. Turrigiano G, LeMasson G, Marder E. Selective regulation of current densities 45. Espinosa JS, Stryker MP. Development and plasticity of the primary visual underlies spontaneous changes in the activity of cultured neurons. J Neurosci. cortex. Neuron. 2012;75(2):230–49. 1995;15(5 Pt 1):3640–52. 46. Dalva MB, Ghosh A, Shatz CJ. Independent control of dendritic and axonal 19. Marder E, Prinz AA. Modeling stability in neuron and network function: the form in the developing lateral geniculate nucleus. J Neurosci. 1994;14(6): role of activity in homeostasis. Bioessays. 2002;24(12):1145–54. 3588–602. 20. Bergquist S, Dickman DK, Davis GW. A hierarchy of cell intrinsic and target- 47. Rocha M, Sur M. Rapid acquisition of dendritic spines by visual thalamic derived homeostatic signaling. Neuron. 2010;66(2):220–34. neurons after blockade of N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A. 1995;92(17):8026–30. 21. Kim EZ, Vienne J, Rosbash M, Griffith LC. Nonreciprocal homeostatic compensation in Drosophila potassium channel mutants. J Neurophysiol. 2017; 48. Pak DT, Sheng M. Targeted protein degradation and synapse remodeling by 117(6):2125–36. an inducible protein kinase. Science. 2003;302(5649):1368–73. 22. Desai NS, Rutherford LC, Turrigiano GG. Plasticity in the intrinsic excitability 49. Seeburg DP, Sheng M. Activity-induced polo-like kinase 2 is required for of cortical pyramidal neurons. Nat Neurosci. 1999;2(6):515–20. homeostatic plasticity of hippocampal neurons during epileptiform activity. 23. Schulz DJ, Goaillard JM, Marder E. Variable channel expression in identified J Neurosci. 2008;28(26):6583–91. single and electrically coupled neurons in different animals. Nat Neurosci. 50. Lee KJ, Lee Y, Rozeboom A, Lee JY, Udagawa N, Hoe HS, Pak DT. Requirement 2006;9(3):356–62. for Plk2 in orchestrated ras and rap signaling, homeostatic structural plasticity, 24. Golowasch J, Goldman MS, Abbott LF, Marder E. Failure of averaging in the and memory. Neuron. 2011;69(5):957–73. construction of a conductance-based neuron model. J Neurophysiol. 2002; 51. Chen C, Regehr WG. Developmental remodeling of the retinogeniculate 87(2):1129–31. synapse. Neuron. 2000;28(3):955–66. 52. Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W. Structural and 25. Schulz DJ. Plasticity and stability in neuronal output via changes in intrinsic excitability: it's what's inside that counts. J Exp Biol. 2006;209(Pt functional composition of the developing retinogeniculate pathway in the 24):4821–7. mouse. Vis Neurosci. 2005;22(5):661–76. 26. O'Leary T, Williams AH, Caplan JS, Marder E. Correlations in ion channel 53. Hooks BM, Chen C. Distinct roles for spontaneous and visual activity in expression emerge from homeostatic tuning rules. Proc Natl Acad Sci U S A. remodeling of the retinogeniculate synapse. Neuron. 2006;52(2):281–91. 2013;110(28):E2645–54. 54. Lin DJ, Kang E, Chen C. Changes in input strength and number are driven 27. Hudson AE, Prinz AA. Conductance ratios and cellular identity. PLoS by distinct mechanisms at the retinogeniculate synapse. J Neurophysiol. Comput Biol. 2010;6(7):e1000838. 2014;112(4):942–50. 28. Grubb MS, Burrone J. Activity-dependent relocation of the axon initial 55. Davis GW, Muller M. Homeostatic control of presynaptic neurotransmitter segment fine-tunes neuronal excitability. Nature. 2010;465(7301):1070–4. release. Annu Rev Physiol. 2015;77:251–70. 29. Kuba H, Oichi Y, Ohmori H. Presynaptic activity regulates Na(+) channel 56. Burrone J, Murthy VN. Synaptic gain control and homeostasis. Curr Opin distribution at the axon initial segment. Nature. 2010;465(7301):1075–8. Neurobiol. 2003;13(5):560–7. 30. Evans MD, Dumitrescu AS, Kruijssen DLH, Taylor SE, Grubb MS. Rapid 57. Oleskevich S, Walmsley B. Synaptic transmission in the auditory brainstem modulation of axon initial segment length influences repetitive spike of normal and congenitally deaf mice. J Physiol. 2002;540(Pt 2):447–55. firing. Cell Rep. 2015;13(6):1233–45. 58. Echegoyen J, Neu A, Graber KD, Soltesz I. Homeostatic plasticity studied 31. Yin J, Yuan Q. Structural homeostasis in the nervous system: a balancing act using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic for wiring plasticity and stability. Front Cell Neurosci. 2014;8:439. plasticity and age-dependence. PLoS One. 2007;2(8):e700. 32. Gutzmann A, Ergul N, Grossmann R, Schultz C, Wahle P, Engelhardt M. A 59. Lambo ME, Turrigiano GG. Synaptic and intrinsic homeostatic mechanisms period of structural plasticity at the axon initial segment in developing cooperate to increase L2/3 pyramidal neuron excitability during a late phase of visual cortex. Front Neuroanat. 2014;8:11. critical period plasticity. J Neurosci. 2013;33(20):8810–9. 33. Petersen AV, Cotel F, Perrier JF. Plasticity of the axon initial segment: fast 60. Slomowitz E, Styr B, Vertkin I, Milshtein-Parush H, Nelken I, Slutsky M, Slutsky and slow processes with multiple functional roles. Neuroscientist. 2016;23(4): I. Interplay between population firing stability and single neuron dynamics 364–73. in hippocampal networks. elife. 2015;4:e04378. 34. Temporal S, Lett KM, Schulz DJ. Activity-dependent feedback regulates 61. Pozo K, Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. correlated ion channel mRNA levels in single identified motor neurons. Neuron. 2010;66(3):337–51. Current biology : CB. 2014;24(16):1899–904. 62. Chattopadhyaya B, Di Cristo G, Higashiyama H,Knott GW,Kuhlman SJ,WelkerE, 35. Zhang W, Linden DJ. The other side of the engram: experience-driven Huang ZJ. Experience and activity-dependent maturation of perisomatic changes in neuronal intrinsic excitability. Nat Rev Neurosci. 2003;4(11): GABAergic innervation in primary visual cortex during a postnatal 885–900. critical period. J Neurosci. 2004;24(43):9598–611. 36. Frick A, Johnston D. Plasticity of dendritic excitability. J Neurobiol. 2005; 63. Marty S, Wehrle R, Sotelo C. Neuronal activity and brain-derived neurotrophic 64(1):100–15. factor regulate the density of inhibitory synapses in organotypic slice cultures 37. Wierenga CJ, Walsh MF, Turrigiano GG. Temporal regulation of the expression of postnatal hippocampus. J Neurosci. 2000;20(21):8087–95. locus of homeostatic plasticity. J Neurophysiol. 2006;96(4):2127–33. 64. Seil FJ, Drake-Baumann R. Reduced cortical inhibitory synaptogenesis in organotypic cerebellar cultures developing in the absence of neuronal 38. Burrone J, O'Byrne M, Murthy VN. Multiple forms of synaptic plasticity activity. J Comp Neurol. 1994;342(3):366–77. triggered by selective suppression of activity in individual neurons. 65. Hartman KN, Pal SK, Burrone J, Murthy VN. Activity-dependent regulation of Nature. 2002;420(6914):414–8. inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci. 39. Kaneko M, Stryker MP. Homeostatic plasticity mechanisms in mouse V1. 2006;9(5):642–9. Philos Trans R Soc Lond Ser B Biol Sci. 2017;372(1715). https://doi.org/10. 1098/rstb.2016.0504. 66. Jiao Y, Zhang C, Yanagawa Y, Sun QQ. Major effects of sensory experiences 40. Johnson RE, Tien NW, Shen N, Pearson JT, Soto F, Kerschensteiner D. Homeostatic on the neocortical inhibitory circuits. J Neurosci. 2006;26(34):8691–701. plasticity shapes the visual system's first synapse. Nat Commun. 2017;8(1):1220. 67. Flores CE, Mendez P. Shaping inhibition: activity dependent structural 41. Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms plasticity of GABAergic synapses. Front Cell Neurosci. 2014;8:327. for stabilizing neuronal function. Cold Spring Harb Perspect Biol. 2012;4(1): 68. Rutherford LC, Nelson SB, Turrigiano GG. BDNF has opposite effects on the a005736. quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron. 1998;21(3):521–30. 42. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci. 69. Maffei A, Nataraj K, Nelson SB, Turrigiano GG. Potentiation of cortical 2002;5(8):783–9. inhibition by visual deprivation. Nature. 2006;443(7107):81–4. 43. Petrus E, Anguh TT, Pho H, Lee A, Gammon N, Lee HK. Developmental switch 70. Maffei A, Turrigiano GG. Multiple modes of network homeostasis in visual in the polarity of experience-dependent synaptic changes in layer 6 of mouse cortical layer 2/3. J Neurosci. 2008;28(17):4377–84. visual cortex. J Neurophysiol. 2011;106(5):2499–505. 71. Borodinsky LN, Belgacem YH, Swapna I, Sequerra EB. Dynamic regulation of 44. Goel A, Lee HK. Persistence of experience-induced homeostatic synaptic neurotransmitter specification: relevance to nervous system homeostasis. plasticity through adulthood in superficial layers of mouse visual cortex. Neuropharmacology. 2014;78:75–80. J Neurosci. 2007;27(25):6692–700. 72. Spitzer NC. Neurotransmitter switching? No surprise. Neuron. 2015;86(5):1131–44. Tien and Kerschensteiner Neural Development (2018) 13:9 Page 7 of 7 73. Spitzer NC. Neurotransmitter switching in the developing and adult brain. 100. Blaesse P, Airaksinen MS, Rivera C, Kaila K. Cation-chloride cotransporters Annu Rev Neurosci. 2017;40:1–19. and neuronal function. Neuron. 2009;61(6):820–38. 74. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. Activity- 101. Gonzalez-Islas C, Wenner P. Spontaneous network activity in the embryonic dependent homeostatic specification of transmitter expression in embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron. neurons. Nature. 2004;429(6991):523–30. 2006;49(4):563–75. 75. Guemez-Gamboa A, Xu L, Meng D, Spitzer NC. Non-cell-autonomous mechanism 102. Gonzalez-Islas C, Chub N, Garcia-Bereguiain MA, Wenner P. GABAergic of activity-dependent neurotransmitter switching. Neuron. 2014;82(5):1004–16. synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential. J Neurosci. 2010;30(39):13016–20. 76. TasicB,Menon V, Nguyen TN,Kim TK,JarskyT,Yao Z, Levi B, Gray LT, 103. Torborg CL, Feller MB. Spontaneous patterned retinal activity and the Sorensen SA, Dolbeare T, et al. Adult mouse cortical cell taxonomy refinement of retinal projections. Prog Neurobiol. 2005;76(4):213–35. revealed by single cell transcriptomics. Nat Neurosci. 2016;19(2):335–46. 104. Huberman AD, Wang GY, Liets LC, Collins OA, Chapman B, Chalupa LM. Eye- 77. Cembrowski MS, Wang L, Sugino K, Shields BC, Spruston N. Hipposeq: a specific retinogeniculate segregation independent of normal neuronal activity. comprehensive RNA-seq database of gene expression in hippocampal Science. 2003;300(5621):994–8. principal neurons. elife. 2016;5:e14997. 105. Torborg CL, Hansen KA, Feller MB. High frequency, synchronized bursting 78. Toledo-Rodriguez M, Markram H. Single-cell RT-PCR, a technique to decipher drives eye-specific segregation of retinogeniculate projections. Nat Neurosci. the electrical, anatomical, and genetic determinants of neuronal diversity. 2005;8(1):72–8. Methods Mol Biol. 2007;403:123–39. 106. Giachello CN, Baines RA. Regulation of motoneuron excitability and the 79. Bloodgood BL, Sharma N, Browne HA, Trepman AZ, Greenberg ME. The setting of homeostatic limits. Curr Opin Neurobiol. 2017;43:1–6. activity-dependent transcription factor NPAS4 regulates domain-specific 107. Hobert O. Terminal selectors of neuronal identity. Curr Top Dev Biol. 2016; inhibition. Nature. 2013;503(7474):121–5. 116:455–75. 80. Bartley AF, Huang ZJ, Huber KM, Gibson JR. Differential activity-dependent, 108. Marder E, Goaillard JM. Variability, compensation and homeostasis in neuron homeostatic plasticity of two neocortical inhibitory circuits. J Neurophysiol. and network function. Nat Rev Neurosci. 2006;7(7):563–74. 2008;100(4):1983–94. 109. Giachello CN, Baines RA. Inappropriate neural activity during a sensitive period 81. Pieraut S, Gounko N, Sando R 3rd, Dang W, Rebboah E, Panda S, Madisen L, in embryogenesis results in persistent seizure-like behavior. Current biology : Zeng H, Maximov A. Experience-dependent remodeling of basket cell CB. 2015;25(22):2964–8. networks in the dentate gyrus. Neuron. 2014;84(1):107–22. 110. Truszkowski TL, Aizenman CD. Neurobiology: setting the set point for neural 82. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. Differences between somatic homeostasis. Current biology : CB. 2015;25(23):R1132–3. and dendritic inhibition in the hippocampus. Neuron. 1996;16(4):815–23. 111. Ramocki MB, Zoghbi HY. Failure of neuronal homeostasis results in common 83. Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by neuropsychiatric phenotypes. Nature. 2008;455(7215):912–8. somatic feed-forward inhibition. Science. 2001;293(5532):1159–63. 112. Meredith RM, Dawitz J, Kramvis I. Sensitive time-windows for susceptibility 84. Maffei A, Nelson SB, Turrigiano GG. Selective reconfiguration of layer 4 visual in neurodevelopmental disorders. Trends Neurosci. 2012;35(6):335–44. cortical circuitry by visual deprivation. Nat Neurosci. 2004;7(12):1353–9. 113. Mullins C, Fishell G, Tsien RW. Unifying views of autism Spectrum disorders: 85. Takesian AE, Kotak VC, Sanes DH. Presynaptic GABA(B) receptors regulate a consideration of autoregulatory feedback loops. Neuron. 2016;89(6):1131–56. experience-dependent development of inhibitory short-term plasticity. 114. Vislay RL, Martin BS, Olmos-Serrano JL, Kratovac S, Nelson DL, Corbin JG, J Neurosci. 2010;30(7):2716–27. Huntsman MM. Homeostatic responses fail to correct defective amygdala 86. Takesian AE, Kotak VC, Sharma N, Sanes DH. Hearing loss differentially affects inhibitory circuit maturation in fragile X syndrome. J Neurosci. 2013;33(17): thalamic drive to two cortical interneuron subtypes. J Neurophysiol. 2013; 7548–58. 110(4):999–1008. 87. Tien NW, Soto F, Kerschensteiner D. Homeostatic plasticity shapes cell-type- specific wiring in the retina. Neuron. 2017;94(3):656–65. e654 88. Blankenship AG, Feller MB. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci. 2010;11(1):18–29. 89. Kerschensteiner D. Spontaneous network activity and synaptic development. J Neurosci. 2014;20(3):272–90. 90. Ackman JB, Burbridge TJ, Crair MC. Retinal waves coordinate patterned activity throughout the developing visual system. Nature. 2012;490(7419):219–25. 91. Assali A, Gaspar P, Rebsam A. Activity dependent mechanisms of visual map formation–from retinal waves to molecular regulators. Semin Cell Dev Biol. 2014;35:136–46. 92. Arroyo DA, Feller MB. Spatiotemporal features of retinal waves instruct the wiring of the visual circuitry. Front Neural Circuits. 2016;10:54. 93. Stacy RC, Demas J, Burgess RW, Sanes JR, Wong RO. Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci. 2005; 25(41):9347–57. 94. Sun C, Warland DK, Ballesteros JM, van der List D, Chalupa LM: Retinal waves in mice lacking the beta2 subunit of the nicotinic acetylcholine receptor. Proc Natl Acad Sci U S A 2008, 105(36):13638–13643. 95. Stafford BK, Sher A, Litke AM, Feldheim DA. Spatial-temporal patterns of retinal waves underlying activity-dependent refinement of retinofugal projections. Neuron. 2009;64(2):200–12. 96. Bansal A, Singer JH, Hwang BJ, Xu W, Beaudet A, Feller MB. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci. 2000;20(20):7672–81. 97. Blankenship AG, Ford KJ, Johnson J, Seal RP, Edwards RH, Copenhagen DR, Feller MB. Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron. 2009;62(2):230–41. 98. Wenner P. Homeostatic synaptic plasticity in developing spinal networks driven by excitatory GABAergic currents. Neuropharmacology. 2014;78:55–62. 99. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev. 2007;87(4):1215–84.
Neural Development – Springer Journals
Published: Jun 1, 2018
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