Deprivation-induced strengthening of presynaptic and postsynaptic inhibitory transmission in layer 4 of visual cortex during the critical period

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2571-2582

  Nahmani, Marc ^a   Turrigiano, Gina G ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Electron microscopy; Fast spiking; LTP; Monocular deprivation; Optogenetic; Pyramidal

Indexed keywords

ELECTRON MICROSCOPY; FAST-SPIKING; LTP; MONOCULAR DEPRIVATION; OPTOGENETIC; PYRAMIDAL;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; SYNAPSES; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 84893684327     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4600-13.2014     Document Type: Article

References (79)

1. Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159-170. CrossRef Medline
2. Bosch M, Hayashi Y (2012) Structural plasticity of dendritic spines. Curr Opin Neurobiol 22:383-388. CrossRef Medline
3. Branco T, Marra V, Staras K (2010) Examining size-strength relationships at hippocampal synapses using an ultrastructural measurement of synaptic release probability. J Struct Biol 172:203-210. CrossRef Medline
4. Castillo PE, Chiu CQ, Carroll RC (2011) Long-term plasticity at inhibitory synapses. Curr Opin Neurobiol 21:328-338. CrossRef Medline
5. Cellerino A, Siciliano R, Domenici L, Maffei L (1992) Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience 51:749-753. CrossRef Medline
6. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611. CrossRef Medline
7. Coleman JE, Nahmani M, Gavornik JP, Haslinger R, Heynen AJ, Erisir A, Bear MF (2010) Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. J Neurosci 30:9670-9682. CrossRef Medline
8. Czeiger D, White EL (1997) Comparisonof the distribution of parvalbuminimmunoreactive and other synapses onto the somata of callosal projection neurons in mouse visual and somatosensory cortex. J Comp Neurol 379:198-210. CrossRef Medline
9. Darcy KJ, Staras K, Collinson LM, Goda Y (2006) Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9:315-321. CrossRef Medline
10. de la Rocha J, Marchetti C, Schiff M, Reyes AD (2008) Linking the response properties of cells in auditory cortex with network architecture: cotuning versus lateral inhibition. J Neurosci 28:9151-9163. CrossRef Medline
11. De Felipe J, Fairén A (1982) A type of basket cell in superficial layers of the cat visual cortex. A Golgi-electron microscope study. Brain Res 244:9-16. CrossRef Medline
12. Desmond NL, Levy WB (1983) Synaptic correlates of associative potentiation/ depression: an ultrastructural study in the hippocampus. Brain Res 265:21-30. CrossRef Medline
13. Essrich C, Lorez M, Benson JA, Fritschy JM, Lüscher B (1998) Postsynaptic clustering of major GABAAreceptor subtypes requires the γ2 subunit and gephyrin. Nat Neurosci 1:563-571. CrossRef Medline
14. Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60:1288-1294. CrossRef Medline
15. Fagiolini M, Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404:183-186. CrossRef Medline
16. Fernández-Busnadiego R, Zuber B, Maurer UE, Cyrklaff M, Baumeister W, Lucic V (2010) Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J Cell Biol 188:145-156. CrossRef Medline
17. Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61. CrossRef Medline
18. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327. CrossRef Medline
19. Hainfeld JF, Furuya FR (1992) A 1.4-nm gold cluster covalently attached to antibodies improves immunolabeling. J Histochem Cytochem 40:177-184. CrossRef Medline
20. Harris KM, Fiala JC, Ostroff L (2003) Structural changes at dendritic spine synapses during long-term potentiation. Philos Trans R Soc Lond B Biol Sci 358:745-748. CrossRef Medline
21. Harris KM, Perry E, Bourne J, Feinberg M, Ostroff L, Hurlburt J (2006) Uniform serial sectioning for transmission electron microscopy. J Neurosci 26:12101-12103. CrossRef Medline
22. Harris LJ, Larson SB, Hasel KW, Day J, Greenwood A, McPherson A (1992) The three-dimensional structure of an intact monoclonal antibody for canine lymphoma. Nature 360:369-372. CrossRef Medline
23. Hengen KB, Lambo ME, Van Hooser SD, Katz DB, Turrigiano GG (2013) Firing rate homeostasis in visual cortex of freely behaving rodents. Neuron 80:335-342. CrossRef Medline
24. Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 126:1345-1347. CrossRef Medline
25. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508. CrossRef Medline
26. Hill TC, Zito K (2013) LTP-induced long-term stabilization of individual nascent dendritic spines. J Neurosci 33:678-686. CrossRef Medline
27. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLo S Biol 3:e159. CrossRef Medline
28. Holderith N, Lorincz A, Katona G, Rózsa B, Kulik A, Watanabe M, Nusser Z (2012) Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci 15:988-997. CrossRef Medline
29. Holländer H, Vanegas H (1981) Identification of pericellular baskets in the cat striate cortex: light and electron microscopic observations after uptake of horseradish peroxidase. J Neurocytol 10:577-587. CrossRef Medline
30. Holmgren CD, Zilberter Y (2001) Coincident spiking activity induces longterm changes in inhibition of neocortical pyramidal cells. J Neurosci 21: 8270-8277. Medline
31. House DR, Elstrott J, Koh E, Chung J, Feldman DE (2011) Parallel regulation of feedforward inhibition and excitation during whisker map plasticity. Neuron 72:819-831. CrossRef Medline
32. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755. CrossRef Medline
33. Inagaki T, Begum T, Reza F, Horibe S, Inaba M, Yoshimura Y, Komatsu Y (2008) Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons. Neurosci Res 61:192-200. CrossRef Medline
34. Itami C, Kimura F, Nakamura S (2007) Brain-derived neurotrophic factor regulates the maturation of layer 4 fast-spiking cells after the second postnatal week in the developing barrel cortex. J Neurosci 27:2241-2252. CrossRef Medline
35. Iwai Y, Fagiolini M, Obata K, Hensch TK (2003) Rapid critical period induction by tonic inhibition in visual cortex. J Neurosci 23:6695-6702. Medline
36. Jiang B, Sohya K, Sarihi A, Yanagawa Y, Tsumoto T (2010) Laminar-specific maturation of GABAergic transmission and susceptibility to visual deprivation are related to endocannabinoid sensitivity in mouse visual cortex. J Neurosci 30:14261-14272. CrossRef Medline
37. Jiao Y, Zhang C, Yanagawa Y, Sun QQ (2006) Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 26:8691-8701. CrossRef Medline
38. Kuhlman SJ, Olivas ND, Tring E, Ikrar T, Xu X, Trachtenberg JT (2013) A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501:543-546. CrossRef Medline
39. Kullmann DM, Ruiz A, Rusakov DM, Scott R, Semyanov A, Walker MC (2005) Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog Biophys Mol Biol 87:33-46. CrossRef Medline
40. Lamsa KP, Kullmann DM, Woodin MA (2010) Spike-timing-dependent plasticity in inhibitory circuits. Front Synaptic Neurosci 2:8. Medline
41. Larkman A, Hannay T, Stratford K, Jack J (1992) Presynaptic release probability influences the locus of long-term potentiation. Nature 360:70-73. CrossRef Medline
42. Lazarus MS, Huang ZJ (2011) Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period for ocular dominance plasticity. J Neurophysiol 106:775-787. CrossRef Medline
43. Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES, Deisseroth K, Dan Y (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379-383. CrossRef Medline
44. Lefort S, Gray AC, Turrigiano GG (2013) Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period. Proc Natl Acad Sci U S A 110:E4540-4547. CrossRef Medline
45. Liu Y, Zhang LI, Tao HW (2007) Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J Neurosci 27:5301-5312. CrossRef Medline
46. Luscher B, Fuchs T, Kilpatrick CL (2011) GABAA receptor traffickingmediated plasticity of inhibitory synapses. Neuron 70:385-409. CrossRef Medline
47. Ma Y, Hu H, Agmon A (2012) Short-term plasticity of unitary inhibitoryto-inhibitory synapses depends on the presynaptic interneuron subtype. J Neurosci 32:983-988. CrossRef Medline
48. Maffei A (2011) The many forms and functions of long term plasticity at GABAergic synapses. Neural Plast 2011:254724. CrossRef Medline
49. Maffei A, Turrigiano G (2008) The age of plasticity: Developmental regulation of synaptic plasticity in neocortical microcircuits. Prog Brain Res 169:211-223. CrossRef Medline
50. Maffei A, Nelson SB, Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7:1353-1359. CrossRef Medline
51. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443:81-84. CrossRef Medline
52. Maffei A, Lambo ME, Turrigiano GG (2010) Critical period for inhibitory plasticity in rodent binocular V1. J Neurosci 30:3304-3309. CrossRef Medline
53. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766. CrossRef Medline
54. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682. CrossRef Medline
55. Nahmani M, Erisir A (2005) VGlu T2 immunochemistry identifies thalamocortical terminals in layer 4 of adult and developing visual cortex. J Comp Neurol 484:458-473. CrossRef Medline
56. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB (2009) Transcriptional and electrophysiological maturation of neocortical fastspiking GABAergic interneurons. J Neurosci 29:7040-7052. CrossRef Medline
57. Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535-545. CrossRef Medline
58. Pangratz-Fuehrer S, Hestrin S (2011) Synaptogenesis of electrical and GABAergic synapses of fast-spiking inhibitory neurons in the neocortex. J Neurosci 31:10767-10775. CrossRef Medline
59. Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58:441-446. CrossRef Medline
60. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251. CrossRef Medline
61. Reyes AD (2011) Synaptic short-term plasticity in auditory cortical circuits. Hear Res 279:60-66. CrossRef Medline
62. Rutledge LT (1978) The effects of denervation and stimulation upon synaptic ultrastructure. J Comp Neurol 178:117-128. CrossRef Medline
63. Sarihi A, Mirnajafi-Zadeh J, Jiang B, Sohya K, Safari MS, Arami MK, Yanagawa Y, Tsumoto T (2012) Cell type-specific, presynaptic LTP of inhibitory synapses on fast-spiking GABAergic neurons in the mouse visual cortex. J Neurosci 32:13189-13199. CrossRef Medline
64. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to Image J: 25 years of image analysis. Nat Methods 9:671-675. CrossRef Medline
65. Siksou L, Triller A, Marty S (2011) Ultrastructural organization of presynaptic terminals. Curr Opin Neurobiol 21:261-268. CrossRef Medline
66. Sjöström PJ, Turrigiano GG, Nelson SB (2007) Multiple forms of long-term plasticity at unitary neocortical layer 5 synapses. Neuropharmacology 52:176-184. CrossRef Medline
67. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702. CrossRef Medline
68. Somogyi P, Kisvárday ZF, Martin KA, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261-294. CrossRef Medline
69. Southwell DG, Froemke RC, Alvarez-Buylla A, Stryker MP, Gandhi SP (2010) Cortical plasticity induced by inhibitory neuron transplantation. Science 327:1145-1148. CrossRef Medline
70. Varela JA, Song S, Turrigiano GG, Nelson SB (1999) Differential depression at excitatory and inhibitory synapses in visual cortex. J Neurosci 19:4293-4304. Medline
71. Vogels TP, Froemke RC, Doyon N, Gilson M, Haas JS, Liu R, Maffei A, Miller P, Wierenga CJ, Woodin MA, Zenke F, Sprekeler H (2013) Inhibitory synaptic plasticity: spike timing-dependence and putative network function. Front Neural Circuits 7:119. Medline
72. Wang XB, Yang Y, Zhou Q (2007) Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27:12419-12429. CrossRef Medline
73. Werner TC, Bunting JR, Cathou RE (1972) The shape of immunoglobulin G molecules in solution. Proc Natl Acad Sci U S A 69:795-799. CrossRef Medline
74. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615. CrossRef Medline
75. Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343-348. CrossRef Medline
76. Wu H, Jin Y, Buddhala C, Osterhaus G, Cohen E, Jin H, Wei J, Davis K, Obata K, Wu JY (2007) Role of glutamate decarboxylase (GAD) isoform, GAD65, in GABA synthesis and transport into synaptic vesicles: evidence from GAD65-knockout mice studies. Brain Res 1154:80-83. CrossRef Medline
77. Yazaki-Sugiyama Y, Kang S, Câteau H, Fukai T, Hensch TK (2009) Bidirectional plasticity in fast-spiking GABAcircuits by visual experience. Nature 462:218-221. CrossRef Medline
78. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089. CrossRef Medline
79. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44: 749-757. CrossRef Medline