The dialectic of Hebb and homeostasis

Gina Turrigiano

Department of Biology, Brandeis University, Waltham, MA 02493, USA

e-mail: ude.siednarb@onaigirrut

One contribution of 16 to a discussion meeting issue ‘Integrating Hebbian and homeostatic plasticity’.

Department of Biology, Brandeis University, Waltham, MA 02493, USA

One contribution of 16 to a discussion meeting issue ‘Integrating Hebbian and homeostatic plasticity’.

Accepted 2016 Jul 7.

Abstract

It has become widely accepted that homeostatic and Hebbian plasticity mechanisms work hand in glove to refine neural circuit function. Nonetheless, our understanding of how these fundamentally distinct forms of plasticity compliment (and under some circumstances interfere with) each other remains rudimentary. Here, I describe some of the recent progress of the field, as well as some of the deep puzzles that remain. These include unravelling the spatial and temporal scales of different homeostatic and Hebbian mechanisms, determining which aspects of network function are under homeostatic control, and understanding when and how homeostatic and Hebbian mechanisms must be segregated within neural circuits to prevent interference.

This article is part of the themed issue ‘Integrating Hebbian and homeostatic plasticity’.

Keywords: synaptic scaling, homeostatic plasticity, Hebbian plasticity, sleep

Abstract

Acknowledgements

I thank many co-workers and collaborators—including Sacha Nelson, Eve Marder, Larry Abbott and all the members of the Turrigiano laboratory past and present—for contributing to the evolution of my ideas about the function of homeostatic mechanisms.

Acknowledgements

Endnote

^{We maintain a small shrine devoted to reviewer 3. In all fairness to reviewers 1 and 2, the manuscript was dramatically improved in response to their critiques.}

Endnote

References

1. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998 Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature391, 892–896. (10.1038/36103) [] [[PubMed][Google Scholar]
2. Stellwagen D. (ed.). 2014. Homeostatic synaptic plasticity. Neuropharmacology78, 1–80. [PubMed]
3. Turrigiano GG. 2008 The self-tuning neuron: synaptic scaling of excitatory synapses. Cell135, 422–435. (10.1016/j.cell.2008.10.008) ] [[Google Scholar]
4. Turrigiano GG, Nelson SB. 2004 Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci.5, 97–107. (10.1038/nrn1327) [] [[PubMed][Google Scholar]
5. Pozo K, Goda Y. 2010 Unraveling mechanisms of homeostatic synaptic plasticity. Neuron66, 337–351. (10.1016/j.neuron.2010.04.028) ] [[Google Scholar]
6. Davis GW. 2006 Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 29, 307–323. (10.1146/annurev.neuro.28.061604.135751) [] [[PubMed][Google Scholar]
7. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG. 2002 Critical periods for experience-dependent synaptic scaling in visual cortex. Nat. Neurosci. 5, 783–789. (10.1038/nn878) [] [[PubMed][Google Scholar]
8. Goel A, Lee HK. 2007 Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J. Neurosci. 27, 6692–6700. (10.1523/JNEUROSCI.5038-06.2007) ] [[Google Scholar]
9. Lambo ME, Turrigiano GG. 2013 Synaptic and intrinsic homeostatic mechanisms cooperate to increase L2/3 pyramidal neuron excitability during a late phase of critical period plasticity. J. Neurosci. 33, 8810–8819. (10.1523/JNEUROSCI.4502-12.2013) ] [[Google Scholar]
10. Hengen KB, Lambo ME, Van Hooser SD, Katz DB, Turrigiano GG. 2013 Firing rate homeostasis in visual cortex of freely behaving rodents. Neuron80, 335–342. (10.1016/j.neuron.2013.08.038) ] [[Google Scholar]
11. Keck T, Keller GB, Jacobsen RI, Eysel UT, Bonhoeffer T, Hubener M. 2013 Synaptic scaling and homeostatic plasticity in the mouse visual cortex in vivo. Neuron80, 327–334. (10.1016/j.neuron.2013.08.018) [] [[PubMed][Google Scholar]
12. Burrone J, O'Byrne M, Murthy VN. 2002 Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature420, 414–418. (10.1038/nature01242) [] [[PubMed][Google Scholar]
13. Slomowitz E, Styr B, Vertkin I, Milshtein-Parush H, Nelken I, Slutsky M, Slutsky I. 2015 Interplay between population firing stability and single neuron dynamics in hippocampal networks. eLife4, e04378 (10.7554/eLife.04378) ] [[Google Scholar]
14. Hengen KB, Torrado Pacheco A, McGregor JN, Van Hooser SD, Turrigiano GG. 2016 Neuronal firing rate homeostasis is inhibited by sleep and promoted by wake. Cell165, 180–191. (10.1016/j.cell.2016.01.046) ] [[Google Scholar]
15. Ibata K, Sun Q, Turrigiano GG. 2008 Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron57, 819–826. (10.1016/j.neuron.2008.02.031) [] [[PubMed][Google Scholar]
16. Gainey MA, Hurvitz-Wolff JR, Lambo ME, Turrigiano GG. 2009 Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J. Neurosci.29, 6479–6489. [Google Scholar]
17. Gainey MA, Tatavarty V, Nahmani M, Lin H, Turrigiano GG. 2015 Activity-dependent synaptic GRIP1 accumulation drives synaptic scaling up in response to action potential blockade. Proc. Natl Acad. Sci. USA112, E3590–E3599. (10.1073/pnas.1510754112) ] [[Google Scholar]
18. Bourne JN, Chirillo MA, Harris KM. 2013 Presynaptic ultrastructural plasticity along CA3 → CA1 axons during long-term potentiation in mature hippocampus. J. Comp. Neurol. 521, 3898–3912. [Google Scholar]
19. Branco T, Staras K, Darcy KJ, Goda Y. 2008 Local dendritic activity sets release probability at hippocampal synapses. Neuron59, 475–485. (10.1016/j.neuron.2008.07.006) ] [[Google Scholar]
20. Beique JC, Na Y, Kuhl D, Worley PF, Huganir RL. 2011 Arc-dependent synapse-specific homeostatic plasticity. Proc. Natl Acad. Sci. USA108, 816–821. (10.1073/pnas.1017914108) ] [[Google Scholar]
21. Hou Q, Man HY. 2012 Input-specific homeostatic regulation of AMPA receptor accumulation at central synapses. Commun. Integr. Biol. 5, 553–556. (10.4161/cib.22076) ] [[Google Scholar]
22. Desai NS, Rutherford LC, Turrigiano GG. 1999 BDNF regulates the intrinsic excitability of cortical neurons. Learn. Mem. 6, 284–291. [Google Scholar]
23. Kilman V, van Rossum MC, Turrigiano GG. 2002 Activity-deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. J. Neurosci. 22, 1328–1337. [Google Scholar]
24. Rutherford LC, Nelson SB, Turrigiano GG. 1998 BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron21, 521–530. (10.1016/S0896-6273(00)80563-2) [] [[PubMed][Google Scholar]
25. Kim J, Tsien RW. 2008 Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron58, 925–937. (10.1016/j.neuron.2008.05.009) ] [[Google Scholar]
26. Maffei A, Nelson SB, Turrigiano GG. 2004 Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat. Neurosci. 7, 1353–1359. (10.1038/nn1351) [] [[PubMed][Google Scholar]
27. Greenhill SD, Ranson A, Fox K. 2015 Hebbian and homeostatic plasticity mechanisms in regular spiking and intrinsic bursting cells of cortical layer 5. Neuron88, 539–552. (10.1016/j.neuron.2015.09.025) ] [[Google Scholar]
28. Maffei A, Turrigiano GG. 2008 Multiple modes of network homeostasis in visual cortical layer 2/3. J. Neurosci. 28, 4377–4384. (10.1523/JNEUROSCI.5298-07.2008) ] [[Google Scholar]
29. Abbott LF, Nelson SB. 2000 Synaptic plasticity: taming the beast. Nat. Neurosci. 3, 1178–1183. (10.1038/81453) [] [[PubMed][Google Scholar]
30. Cannon WB. 1932 The wisdom of the body. New York, NY: W.W. Norton Co., Inc. [PubMed][Google Scholar]
31. Chistiakova M, Bannon NM, Chen JY, Bazhenov M, Volgushev M. 2015 Homeostatic role of heterosynaptic plasticity: models and experiments. Front. Comput. Neurosci. 9, 89 (10.3389/fncom.2015.00089) ] [[Google Scholar]
32. Bourne JN, Harris KM. 2011 Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus21, 354–373. (10.1002/hipo.20768) ] [[Google Scholar]
33. Kaneko M, Stellwagen D, Malenka RC, Stryker MP. 2008 Tumor necrosis factor-α mediates one component of competitive, experience-dependent plasticity in developing visual cortex. Neuron58, 673–680. (10.1016/j.neuron.2008.04.023) ] [[Google Scholar]
34. Miller KD, MacKay DJC. 1994 The role of constraints in Hebbian learning. Neural Comput. 6, 100–124. (10.1162/neco.1994.6.1.100) [[PubMed][Google Scholar]
35. Toyoizumi T, Kaneko M, Stryker MP, Miller KD. 2014 Modeling the dynamic interaction of Hebbian and homeostatic plasticity. Neuron84, 497–510. (10.1016/j.neuron.2014.09.036) ] [[Google Scholar]
36. Harnack D, Pelko M, Chaillet A, Chitour Y, van Rossum MC. 2015 Stability of neuronal networks with homeostatic regulation. PLoS Comput. Biol. 11, e1004357 (10.1371/journal.pcbi.1004357) ] [[Google Scholar]
37. Wierenga CJ, Ibata K, Turrigiano GG. 2005 Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci. 25, 2895–2905. (10.1523/JNEUROSCI.5217-04.2005) ] [[Google Scholar]
38. Espinosa JS, Stryker MP. 2012 Development and plasticity of the primary visual cortex. Neuron75, 230–249. (10.1016/j.neuron.2012.06.009) ] [[Google Scholar]
39. Maffei A, Nataraj K, Nelson SB, Turrigiano GG. 2006 Potentiation of cortical inhibition by visual deprivation. Nature443, 81–84. (10.1038/nature05079) [] [[PubMed][Google Scholar]
40. Nahmani M, Turrigiano GG. 2014 Deprivation-induced strengthening of presynaptic and postsynaptic inhibitory transmission in layer 4 of visual cortex during the critical period. J. Neurosci. 34, 2571–2582. (10.1523/JNEUROSCI.4600-13.2014) ] [[Google Scholar]
41. van Rossum MC, Bi GQ, Turrigiano GG. 2000 Stable Hebbian learning from spike timing-dependent plasticity. J. Neurosci. 20, 8812–8821. [Google Scholar]
42. Nelson SB, Turrigiano GG. 2008 Strength through diversity. Neuron60, 477–482. (10.1016/j.neuron.2008.10.020) ] [[Google Scholar]
43. Turrigiano G. 2012 Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4, a005736 (10.1101/cshperspect.a005736) ] [[Google Scholar]
44. Abraham WC, Bear MF. 1996 Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126–130. (10.1016/S0166-2236(96)80018-X) [] [[PubMed][Google Scholar]
45. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG. 2000 Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron26, 659–670. (10.1016/S0896-6273(00)81202-7) [] [[PubMed][Google Scholar]
46. De Roo M, Klauser P, Briner A, Nikonenko I, Mendez P, Dayer A, Kiss JZ, Muller D, Vutskits L. 2009 Anesthetics rapidly promote synaptogenesis during a critical period of brain development. PLoS ONE4, e7043 (10.1371/journal.pone.0007043) ] [[Google Scholar]
47. Murthy VN, Schikorski T, Stevens CF, Zhu Y. 2001 Inactivity produces increases in neurotransmitter release and synapse size. Neuron32, 673–682. (10.1016/S0896-6273(01)00500-1) [] [[PubMed][Google Scholar]
48. Tatavarty V, Sun Q, Turrigiano GG. 2013 How to scale down postsynaptic strength. J. Neurosci. 33, 13 179–13 189. (10.1523/JNEUROSCI.1676-13.2013) ] [[Google Scholar]
49. Tononi G, Cirelli C. 2014 Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron81, 12–34. (10.1016/j.neuron.2013.12.025) ] [[Google Scholar]
50. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G. 2009 Cortical firing and sleep homeostasis. Neuron63, 865–878. (10.1016/j.neuron.2009.08.024) ] [[Google Scholar]
51. Xie L, et al. 2013. Sleep drives metabolite clearance from the adult brain. Science342, 373–377. (10.1126/science.1241224) ] [
52. Liu ZW, Faraguna U, Cirelli C, Tononi G, Gao XB. 2010 Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. J. Neurosci. 30, 8671–8675. (10.1523/JNEUROSCI.1409-10.2010) ] [[Google Scholar]
53. Cirelli C, Gutierrez CM, Tononi G. 2014 Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron41, 35–43. (10.1016/S0896-6273(03)00814-6) [] [[PubMed][Google Scholar]
54. Goold CP, Nicoll RA. 2010 Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron68, 512–528. (10.1016/j.neuron.2010.09.020) ] [[Google Scholar]
55. Steinmetz CC, Turrigiano GG. 2010 Tumor necrosis factor-α signaling maintains the ability of cortical synapses to express synaptic scaling. J. Neurosci. 30, 14 685–14 690. (10.1523/JNEUROSCI.2210-10.2010) ] [[Google Scholar]
56. Aton SJ, Seibt J, Dumoulin M, Jha SK, Steinmetz N, Coleman T, Naidoo N, Frank MG. 2009 Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron61, 454–466. (10.1016/j.neuron.2009.01.007) ] [[Google Scholar]
57. Aton SJ, Broussard C, Dumoulin M, Seibt J, Watson A, Coleman T, Frank MG. 2013 Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons. Proc. Natl Acad. Sci. USA110, 3101–3106. (10.1073/pnas.1208093110) ] [[Google Scholar]
58. Frank MG. 2015 Sleep and synaptic plasticity in the developing and adult brain. Curr. Top. Behav. Neurosci. 25, 123–149. (10.1007/7854_2014_305) [] [[PubMed][Google Scholar]