Highly specific structural plasticity of inhibitory circuits in the adult neocortex

Neuroscientist

Volumn 19, Issue 4, 2013, Pages 384-393

  Chen, Jerry L ^a,b   Nedivi, Elly ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

experience dependent plasticity; in vivo imaging; inhibition; structural remodeling; visual cortex

Indexed keywords

BRAIN FUNCTION; HUMAN; INTERNEURON; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION;

EXPERIENCE-DEPENDENT PLASTICITY; IN VIVO IMAGING; INHIBITION; STRUCTURAL REMODELING; VISUAL CORTEX;

ANIMALS; DENDRITES; GAMMA-AMINOBUTYRIC ACID; NEURAL INHIBITION; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 84879935375     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858413479824     Document Type: Review

References (87)

1. Alitto HJ, Dan Y. Function of inhibition in visual cortical processing. Curr Opin Neurobiol. 2010 ; 20 (3). 340-6
2. Arckens L, Schweigart G, Qu Y, Wouters G, Pow DV, Vandesande F. Cooperative changes in GABA, glutamate and activity levels: the missing link in cortical plasticity. Eur J Neurosci. 2000 ; 12 (12). 4222-32
3. Artola A, Singer W. Long-term potentiation and NMDA receptors in rat visual cortex. Nature. 1987 ; 330 (6149). 649-52
4. Bailey CH, Kandel ER. Structural changes accompanying memory storage. Annu Rev Physiol. 1993 ; 55: 397-426
5. Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Maffei L, Sale A. Brain plasticity and disease: a matter of inhibition. Neural Plast. 2011 2011 ; 2011: 286073
6. Bavelier D, Levi DM, Li RW, Dan Y, Hensch TK. Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J Neurosci. 2010 ; 30 (45). 14964-71
7. Beaulieu C, Somogyi P. Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur J Neurosci. 1990 ; 2 (4). 296-303
8. Bozzi Y, Casarosa S, Caleo M. Epilepsy as a neurodevelopmental disorder. Front Psychiatry. 2012 ; 3: 19
9. Buonomano DV, Merzenich MM. Cortical plasticity: from synapses to maps. Annu Rev Neurosci. 1998 ; 21: 149-86
10. Castrén E, Elgersma Y, Maffei L, Hagerman R. Treatment of neurodevelopmental disorders in adulthood. J Neurosci. 2012 ; 32 (41). 14074-9
11. Catterall WA, Dib-Hajj S, Meisler MH, Pietrobon D. Inherited neuronal ion channelopathies: new windows on complex neurological diseases. J Neurosci. 2008 ; 28 (46). 11768-77
12. Chen JL, Flanders GH, Lee WC, Lin WC, Nedivi E. Inhibitory dendrite dynamics as a general feature of the adult cortical microcircuit. J Neurosci. 2011 ; 31 (35). 12437-43
13. Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci. 2011 ; 14 (5). 587-94
14. Chen JL, Villa KL, Cha JW, So PT, Kubota Y, Nedivi E. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron. 2012 ; 74 (2). 361-73
15. Chiu C, Lur G, Higley MJ 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience. Online ; 2012:
16. Chklovskii DB, Mel BW, Svoboda K. Cortical rewiring and information storage. Nature. 2004 ; 431 (7010). 782-8
17. Dan Y, Poo MM. Spike timing-dependent plasticity of neural circuits. Neuron. 2004 ; 44 (1). 23-30
18. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A. 2005 ; 102 (35). 12560-5
19. Darian-Smith C, Gilbert CD. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J Neurosci. 1995 ; 15 (3). 1631-47
20. Drager UC. Observations on monocular deprivation in mice. J Neurophysiol. 1978 ; 41 (1). 28-42
21. Fagiolini M, Hensch TK. Inhibitory threshold for critical-period activation in primary visual cortex. Nature. 2000 ; 404 (6774). 183-6
22. Feldman DE. Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci. 2009 ; 32: 33-55
23. Feldman DE. The spike-timing dependence of plasticity. Neuron. 2012 ; 75 (4). 556-71
24. Fino E, Packer AM, Yuste R. The logic of inhibitory connectivity in the neocortex. Neuroscientist. 2012 ;:
25. Frenkel MY, Sawtell NB, Diogo AC, Yoon B, Neve RL, Bear MF. Instructive effect of visual experience in mouse visual cortex. Neuron. 2006 ; 51 (3). 339-49
26. Froemke RC, Merzenich MM, Schreiner CE. A synaptic memory trace for cortical receptive field plasticity. Nature. 2007 ; 450 (7168). 425-9
27. Gambino F, Holtmaat A. Spike-timing-dependent potentiation of sensory surround in the somatosensory cortex is facilitated by deprivation-mediated disinhibition. Neuron. 2012 ; 75 (3). 490-502
28. Giannikopoulos DV, Eysel UR. Dynamics and specificity of cortical map reorganization after retinal lesions. Proc Natl Acad Sci U S A. 2006 ; 103 (28). 10805-10
29. Gidon A, Segev I. Principles governing the operation of synaptic inhibition in dendrites. Neuron. 2012 ; 75 (2). 330-41
30. Gilbert CD, Wiesel TN. Receptive field dynamics in adult primary visual cortex. Nature. 1992 ; 356 (6365). 150-2
31. Hanover JL, Huang ZJ, Tonegawa S, Stryker MP. Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J Neurosci. 1999 ; 19 (22). RC40
32. Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci. 2010 ; 30 (1). 361-71
33. He HY, Hodos W, Quinlan EM. Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J Neurosci. 2006 ; 26 (11). 2951-5
34. Hendry SH, Fuchs J, deBlas AL, Jones EG. Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J Neurosci. 1990 ; 10 (7). 2438-50
35. Hendry SH, Huntsman MM, Viñuela A, Möhler H, de Blas AL, Jones EG. GABAA receptor subunit immunoreactivity in primate visual cortex: distribution in macaques and humans and regulation by visual input in adulthood. J Neurosci. 1994 ; 14 (4). 2383-401
36. Hendry SH, Jones EG. Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature. 1986 ; 320 (6064). 750-3
37. Hendry SH, Jones EG. Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron. 1988 ; 1 (8). 701-12
38. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci. 2005 ; 6 (11). 877-88
39. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hübener M. Prior experience enhances plasticity in adult visual cortex. Nat Neurosci. 2006 ; 9 (1). 127-32
40. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hübener M. Experience leaves a lasting structural trace in cortical circuits. Nature. 2009 ; 457 (7227). 313-7
41. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW. Transient and persistent dendritic spines in the neocortex in vivo. Neuron. 2005 ; 45 (2). 279-91
42. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 1999 ; 98 (6). 739-55
43. Hubel DH, Wiesel TN, LeVay S. Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci. 1977 ; 278 (961). 377-409
44. Isaacson JS, Scanziani M. How inhibition shapes cortical activity. Neuron. 2011 ; 72 (2). 231-43
45. Jones EG, Powell TP. Morphological variations in the dendritic spines of the neocortex. J Cell Sci. 1969 ; 5 (2). 509-29
46. Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science. 1990 ; 248 (4952). 229-31
47. Kameyama K, Sohya K, Ebina T, Fukuda A, Yanagawa Y, Tsumoto T. Difference in binocularity and ocular dominance plasticity between GABAergic and excitatory cortical neurons. J Neurosci. 2010 ; 30 (4). 1551-9
48. Kanemoto Y, Matsuzaki M, Morita S, Hayama T, Noguchi J, Senda N. Spatial distributions of GABA receptors and local inhibition of Ca2+ transients studied with GABA uncaging in the dendrites of CA1 pyramidal neurons. PloS One. 2011 ; 6 (7). e22652
49. Kawaguchi Y, Karube F, Kubota Y. Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb Cortex. 2006 ; 16 (5). 696-711
50. Kawaguchi Y, Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 1997 ; 7 (6). 476-86
51. Kawaguchi Y, Kubota Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience. 1998 ; 85 (3). 677-701
52. Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, Bonhoeffer T. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron. 2011 ; 71 (5). 869-82
53. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci. 2004 ; 24 (37). 8153-60
54. Knott GW, Quairiaux C, Genoud C, Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 2002 ; 34 (2). 265-73
55. Kubota Y, Hatada S, Kondo S, Karube F, Kawaguchi Y. Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J Neurosci. 2007 ; 27 (5). 1139-50
56. Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT. A dynamic zone defines interneuron remodeling in the adult neocortex. Proc Natl Acad Sci U S A. 2008 ; 105 (50). 19968-73
57. Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol. 2006 ; 4 (2). e29
58. Levelt CN, Hubener M. Critical-period plasticity in the visual cortex. Annu Rev Neurosci. 2012 ; 35: 309-30
59. Maffei A, Nelson SB, Turrigiano GG. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci. 2004 ; 7 (12). 1353-9
60. Maffei A, Turrigiano GG. Multiple modes of network homeostasis in visual cortical layer 2/3. J Neurosci. 2008 ; 28 (17). 4377-84
61. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 1997 ; 275 (5297). 209-13
62. Majewska AK, Newton JR, Sur M. Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci. 2006 ; 26 (11). 3021-9
63. Marik SA, Yamahachi H, McManus JN, Szabo G, Gilbert CD. Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 2010 ; 8 (6). e1000395
64. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 2004 ; 5 (10). 793-807
65. Marsden KC, Shemesh A, Bayer KU, Carroll RC. Selective translocation of Ca2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc Natl Acad Sci U S A. 2010 ; 107 (47). 20559-64
66. Massie A, Cnops L, Smolders I, Van Damme K, Vandenbussche E, Vandesande F. Extracellular GABA concentrations in area 17 of cat visual cortex during topographic map reorganization following binocular central retinal lesioning. Brain Res. 2003 ; 976 (1). 100-8
67. Maya Vetencourt JF, Sale A, Viegi A, Baroncelli L, De Pasquale R, O'Leary OF. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science. 2008 ; 320 (5874). 385-8
68. McBain CJ, Fisahn A. Interneurons unbound. Nat Rev Neurosci. 2001 ; 2 (1). 11-23
69. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF. Differences between somatic and dendritic inhibition in the hippocampus. Neuron. 1996 ; 16 (4). 815-23
70. Mizrahi A, Katz LC. Dendritic stability in the adult olfactory bulb. Nat Neurosci. 2003 ; 6 (11). 1201-7
71. Poirazi P, Mel BW. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron. 2001 ; 29 (3). 779-96
72. Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science. 2001 ; 293 (5532). 1159-63
73. Rubenstein JL, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003 ; 2 (5). 255-67
74. Sale A, Maya Vetencourt JF, Medini P, Cenni MC, Baroncelli L, De Pasquale R. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci. 2007 ; 10 (6). 679-81
75. Sato M, Stryker MP. Distinctive features of adult ocular dominance plasticity. J Neurosci. 2008 ; 28 (41). 10278-86
76. Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron. 2003 ; 38 (6). 977-85
77. Schmid LM, Rosa MG, Calford MB, Ambler JS. Visuotopic reorganization in the primary visual cortex of adult cats following monocular and binocular retinal lesions. Cereb Cortex. 1996 ; 6 (3). 388-405
78. Singer W. Neurophysiology: the changing face of inhibition. Curr Biol. 1996 ; 6 (4). 395-7
79. Somogyi P, Tamás G, Lujan R, Buhl EH. Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev. 1998 ; 26 (2-3). 113-35
80. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci. 2008 ; 9 (3). 206-21
81. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature. 2002 ; 420 (6917). 788-94
82. van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, Sommeijer JP. Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron. 2012 ; 74 (2). 374-83
83. Wierenga CJ, Becker N, Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat Neurosci. 2008 ; 11 (9). 1044-52
84. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol. 1963 ; 26: 1003-17
85. Wiesel TN, Hubel DH. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol. 1965 ; 28 (6). 1029-40
86. Woodruff AR, Anderson SA, Yuste R. The enigmatic function of chandelier cells. Front Neurosci. 2010 ; 4: 201
87. Zuo Y, Lin A, Chang P, Gan WB. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron. 2005 ; 46 (2). 181-9