Experience-dependent plasticity of the barrel cortex in mice observed with 2-DG brain mapping and c-Fos: Effects of MMP-9 KO

Cerebral Cortex

Volumn 22, Issue 9, 2012, Pages 2160-2170

  Kaliszewska, Aleksandra ^a   Bijata, Monika ^a   Kaczmarek, Leszek ^a   Kossut, Malgorzata ^a,b  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b SWPS UNIVERSITY OF SOCIAL SCIENCES AND HUMANITIES   (Poland)

Author keywords

14C 2 deoxyglucose mapping; barrel cortex; c Fos; matrix metalloproteinase 9; sensory deprivation

Indexed keywords

GELATINASE B; PROTEIN C FOS;

ANIMAL EXPERIMENT; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPERIENCE; FEMALE; IMAGE ANALYSIS; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; VIBRISSA;

ANIMALS; AUTORADIOGRAPHY; BRAIN MAPPING; DEOXYGLUCOSE; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; PROTO-ONCOGENE PROTEINS C-FOS; SENSORY DEPRIVATION; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 84864915955     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr303     Document Type: Article

References (79)

1. Arancio O, Chao MV. 2007. Neurotrophins, synaptic plasticity and dementia. Curr Opin Neurobiol. 17:325-330. (Pubitemid 46880319)
2. Attwell D, Laughlin SB. 2001. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. 21:1133-1145. (Pubitemid 32947479)
3. Bender KJ, Rangel J, Feldman DE. 2003. Development of columnar topography in the excitatory layer 4 to layer 2/3 projection in rat barrel cortex. J Neurosci. 23:8759-8770. (Pubitemid 37176657)
4. Benedetti BL, Glazewski S, Barth AL. 2009. Reliable and precise neuronal firing during sensory plasticity in superficial layers of primary somatosensory cortex. J Neurosci. 29:11817-11827.
5. Bernardo KL, McCasland JS, Woolsey TA. 1990. Local axonal trajectories in mouse barrel cortex. Exp Brain Res. 82:247-253. (Pubitemid 20378083)
6. Bisler S, Schleicher A, Gass P, Stehle JH, Zilles K, Staiger JF. 2002. Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-tobarrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment. J Chem Neuroanat. 23:187-198. (Pubitemid 34171637)
7. Bozdagi O, Nagy V, Kwei KT, Huntley GW. 2007. In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J Neurophysiol. 98:334-344. (Pubitemid 47084824)
8. Bureau I, von Saint Paul F, Svoboda K. 2006. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 4:e382.
9. Cheetham CE, Hammond MS, Edwards CE, Finnerty GT. 2007. Sensory experience alters cortical connectivity and synaptic function site specifically. J Neurosci. 27:3456-3465. (Pubitemid 46515126)
10. Cheetham CE, Hammond MS, McFarlane R, Finnerty GT. 2008. Altered sensory experience induces targeted rewiring of local excitatory connections in mature neocortex. J Neurosci. 28:9249-9260.
11. Chmielowska J, Kossut M, Chmielowski M. 1986. Single vibrissal cortical column in the mouse labeled with 2-deoxyglucose. Exp Brain Res. 63:607-619. (Pubitemid 16036234)
12. Clem RL, Celikel T, Barth AL. 2008. Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science. 319:101-104.
13. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L, Caroni P, Svoboda K. 2006. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron. 49:861-875. (Pubitemid 43376083)
14. Diamond ME, Huang W, Ebner FF. 1994. Laminar comparison of somatosensory cortical plasticity. Science. 265:1885-1888. (Pubitemid 24324248)
15. Dodd J, Jessell TM. 1988. Axon guidance and the patterning of neuronal projections in vertebrates. Science. 242:692-699.
16. Duncan GE, Johnson KB, Breese GR. 1993. Topographic patterns of brain activity in response to swim stress: assessment by 2- deoxyglucose uptake and expression of Fos-like immunoreactivity. J Neurosci. 13:3932-3943. (Pubitemid 23264377)
17. Duncan GE, Moy SS, Knapp DJ, Mueller RA, Breese GR. 1998. Metabolic mapping of the rat brain after subanesthetic doses of ketamine: potential relevance to schizophrenia. Brain Res. 787:181-190. (Pubitemid 28197904)
18. Eells JB, Clough RW, Miller JW, Jobe PC, Browning RA. 2000. Fos expression and 2-deoxyglucose uptake following seizures in developing genetically epilepsy-prone rats. Brain Res Bull. 52:379-389. (Pubitemid 30462209)
19. Filipkowski RK, Rydz M, Berdel B, Morys J, Kaczmarek L. 2000. Tactile experience induces c-fos expression in rat barrel cortex. Learn Mem. 7:116-122. (Pubitemid 30213025)
20. Finnerty GT. 2011. Neocortical rewiring and memory storage. Workshop W14.1 at 8th IBRO World Congress of Neuroscience Florence; July 14-18.
21. Fox K. 1992. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci. 12:1826-1838.
22. Fox K. 2002. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience. 111:799-814. (Pubitemid 34603250)
23. Fox K, Glazewski S, Chen CM, Silva A, Li X. 1996. Mechanisms underlying experience-dependent potentiation and depression of vibrissae responses in barrel cortex. J Physiol Paris. 90:263-269. (Pubitemid 27043075)
24. Frostig RD, Xiong Y, Chen-Bee CH, Kvasnak E, Stehberg J. 2008. Largescale organization of rat sensorimotor cortex based on a motif of large activation spreads. J Neurosci. 28:13274-13284.
25. Gierdalski M, Jablonska B, Smith A, Skangiel-Kramska J, Kossut M. 1999. Deafferentation induced changes in GAD67 and GluR2 mRNA expression in mouse somatosensory cortex. Brain Res Mol Brain Res. 71:111-119. (Pubitemid 29320062)
26. Glazewski S, Benedetti BL, Barth AL. 2007. Ipsilateral whiskers suppress experience-dependent plasticity in the barrel cortex. J Neurosci. 27:3910-3920. (Pubitemid 46557673)
27. Glazewski S, Fox K. 1996. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J Neurophysiol. 75:1714-1729. (Pubitemid 26114075)
28. Herdegen T, Leah JD. 1998. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev. 28:370-490. (Pubitemid 29012678)
29. Herrera DG, Robertson HA. 1996. Activation of c-fos in the brain. Prog Neurobiol. 50:83-107. (Pubitemid 26412595)
30. Hickmott PW, Steen PA. 2005. Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat Neurosci. 8:140-142. (Pubitemid 40194040)
31. Holtmaat A, De Paola V, Wilbrecht L, Knott GW. 2008. Imaging of experience-dependent structural plasticity in the mouse neocortex in vivo. Behav Brain Res. 192:20-25.
32. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. 2006. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature. 441:979-983. (Pubitemid 43980351)
33. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K. 2005. Transient and persistent dendritic spines in the neocortex in vivo. Neuron. 45:279-291. (Pubitemid 40128121)
34. Jablonska B, Gierdalski M, Siucinska E, Skangiel-Kramska J, Kossut M. 1995. Partial blocking of NMDA receptors restricts plastic changes in adult mouse barrel cortex. Behav Brain Res. 66:207-216.
35. Jasinska M, Siucinska E, Cybulska-Klosowicz A, Pyza E, Furness DN, Kossut M, Glazewski S. 2010. Rapid, learning-induced inhibitory synaptogenesis in murine barrel field. J Neurosci. 30:1176-1184.
36. Kaczmarek L, Lapinska-Dzwonek J, Szymczak S. 2002. Matrix metalloproteinases in the adult brain physiology: a link between c-Fos, AP-1 and remodeling of neuronal connections? EMBO J. 21:6643-6648. (Pubitemid 36014536)
37. Kano M, Iino K. 1991. Functional reorganization of adult cat somatosensory cortex is dependent on NMDA receptors. Neuroreport. 2:77-80.
38. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci. 9:1117-1124. (Pubitemid 44306304)
39. Knott GW, Quairiaux C, Genoud C, Welker E. 2002. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 34:265-273. (Pubitemid 34442569)
40. Kossut M, Hand P. 1984. The development of the vibrissal cortical column: a 2-deoxyglucose study in the rat. Neurosci Lett. 46:1-6. (Pubitemid 14149222)
41. Kossut M, Hand PJ, Greenberg J, Hand CL. 1988. Single vibrissal cortical column in SI cortex of rat and its alterations in neonatal and adult vibrissa-deafferented animals: a quantitative 2DG study. J Neurophysiol. 60:829-852.
42. Kossut M, Juliano SL. 1999. Anatomical correlates of representational map reorganization induced by partial vibrissectomy in the barrel cortex of adult mice. Neuroscience. 92:807-817. (Pubitemid 29287528)
43. Lebedev MA, Mirabella G, Erchova I, Diamond ME. 2000. Experiencedependent plasticity of rat barrel cortex: redistribution of activity across barrel-columns. Cereb Cortex. 10:23-31. (Pubitemid 30022829)
44. Li S, Overman JJ, Katsman D, Kozlov SV, Donnelly CJ, Twiss JL, Giger RJ, Coppola G, Geschwind DH, Carmichael ST. 2010. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat Neurosci. 13:1496-1504.
45. Liguz-Lecznar M, Siucinska E, Zakrzewska R, Kossut M. 2011. Impairment of experience-dependent cortical plasticity in aged mice. Neurobiol Aging. 32:1896-1905.
46. Lübke J, Roth A, Feldmeyer D, Sakmann B. 2003. Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cortex. 13:1051-1063. (Pubitemid 37163204)
47. Maier DL, Grieb GM, Stelzner DJ, McCasland JS. 2003. Large-scale plasticity in barrel cortex following repeated whisker trimming in young adult hamsters. Exp Neurol. 184:737-745. (Pubitemid 38182802)
48. Marik SA, Yamahachi H, McManus JN, Szabo G, Gilbert CD. 2010. Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 8:e1000395.
49. McCasland JS, Bernardo KL, Probst KL, Woolsey TA. 1992. Cortical local circuit axons do not mature after early deafferentation. Proc Natl Acad Sci U S A. 89:1832-1836.
50. McCown TJ, Duncan GE, Johnson KB, Breese GR. 1995. Metabolic and functional mapping of the neural network subserving inferior collicular seizure generalization. Brain Res. 701:117-128.
51. Meighan SE, Meighan PC, Choudhury P, Davis CJ, Olson ML, Zornes PA, Wright JW, Harding JW. 2006. Effects of extracellular matrixdegrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J Neurochem. 96:1227-1241.
52. Meyer HS, Wimmer VC, Oberlaender M, de Kock CP, Sakmann B, Helmstaedter M. 2010. Number and laminar distribution of neurons in a thalamocortical projection column of rat vibrissal cortex. Cereb Cortex. 20:2277-2286.
53. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L. 2009. Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci. 29:6007-6012.
54. Michaluk P, Wawrzyniak M, Alot P, Szczot M, Wyrembek P, Mercik K, Medvedev N, Wilczek E, DeRoo M, Zuschratter W, et al. 2011. Influence of matrix metalloproteinase, MMP-9 on dendritic spine morphology. J Cell Sci. 124:3369-3380.
55. Montag-Sallaz M, Baarke A, Montag D. 2003. Aberrant neuronal connectivity in CHL1-deficient mice is associated with altered information processing-related immediate early gene expression. J Neurobiol. 57:67-80. (Pubitemid 37087787)
56. Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, Dzwonek J, Costa RM, Silva AJ, Kaczmarek L, Huntley GW. 2006. Matrix metalloproteinase-9 is required for hippocampal late-phase longterm potentiation and memory. J Neurosci. 26:1923-1934.
57. Niblock MM, Brunso-Bechtold JK, Riddle DR. 2000. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci. 20:4165-4176. (Pubitemid 30365687)
58. Nishijima T, Piriz J, Duflot S, Fernandez AM, Gaitan G, Gomez-Pinedo U, Verdugo JM, Leroy F, Soya H, Nunez A, et al. 2010. Neuronal activity drives localized blood-brain-barrier transport of serum insulin-like growth factor-I into the CNS. Neuron. 67:834-846.
59. Nudo RJ, Masterton RB. 1986. Stimulation-induced [14C]2-deoxyglucose labeling of synaptic activity in the central auditory system. J Comp Neurol. 245:553-565. (Pubitemid 16128827)
60. Okulski P, Jay TM, Jaworski J, Duniec K, Dzwonek J, Konopacki FA, Wilczynski GM, Sanchez-Capelo A, Mallet J, Kaczmarek L. 2007. TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol Psychiatry. 62:359-362. (Pubitemid 47454516)
61. Pellerin L, Magistretti PJ. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A. 91:10625-10629. (Pubitemid 24329051)
62. Rema V, Armstrong-James M, Ebner FF. 1998. Experience-dependent plasticity of adult rat S1 cortex requires local NMDA receptor activation. J Neurosci. 18:10196-10206. (Pubitemid 28543793)
63. Romanic AM, Madri JA. 1994. Extracellular matrix-degrading proteinases in the nervous system. Brain Pathol. 4:145-156. (Pubitemid 24140502)
64. Schubert D, Kotter R, Zilles K, Luhmann HJ, Staiger JF. 2003. Cell typespecific circuits of cortical layer IV spiny neurons. J Neurosci. 23:2961-2970. (Pubitemid 36418632)
65. Schwartz WJ, Smith CB, Davidsen L, Savaki H, Sokoloff L, Mata M, Fink DJ, Gainer H. 1979. Metabolic mapping of functional activity in the hypothalamo-neurohypophysial system of the rat. Science. 205:723-725. (Pubitemid 9253867)
66. Seeds NW, Siconolfi LB, Haffke SP. 1997. Neuronal extracellular proteases facilitate cell migration, axonal growth, and pathfinding. Cell Tissue Res. 290:367-370. (Pubitemid 27470070)
67. Shubayev VI, Myers RR. 2004. Matrix metalloproteinase-9 promotes nerve growth factor-induced neurite elongation but not new sprout formation in vitro. J Neurosci Res. 77:229-239. (Pubitemid 38859407)
68. Siucinska E, Kossut M. 1996. Short-lasting classical conditioning induces reversible changes of representational maps of vibrissae in mouse SI cortex-a 2DG study. Cereb Cortex. 6:506-513.
69. Skangiel-Kramska J, Głazewski S, Jabłońska B, Siucińska E, Kossut M. 1994. Reduction of GABAA receptor binding of [3H]muscimol in the barrel field of mice after peripheral denervation: transient and longlasting effects. Exp Brain Res. 100:39-46. (Pubitemid 24244885)
70. Spolidoro M, Putignano E, Munafo C, Maffei L, Pizzorusso T. 2011. Inhibition of matrix metalloproteinases prevents the potentiation of nondeprived-eye responses after monocular deprivation in juvenile rats. Cereb Cortex. doi: 10.1093/cercor/bhr158.
71. Staiger JF, Bisler S, Schleicher A, Gass P, Stehle JH, Zilles K. 2000. Exploration of a novel environment leads to the expression of inducible transcription factors in barrel-related columns. Neuroscience. 99:7-16. (Pubitemid 30495547)
72. Strominger RN, Woolsey TA. 1987. Templates for locating the whisker area in fresh flattened mouse and rat cortex. J Neurosci Methods. 22:113-118. (Pubitemid 17163167)
73. Tailby C, Wright LL, Metha AB, Calford MB. 2005. Activity-dependent maintenance and growth of dendrites in adult cortex. Proc Natl Acad Sci U S A. 102:4631-4636. (Pubitemid 40397163)
74. Vaillant C, Didier-Bazes M, Hutter A, Belin MF, Thomasset N. 1999. Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci. 19:4994-5004. (Pubitemid 29270134)
75. Wallace H, Fox K. 1999. The effect of vibrissa deprivation pattern on the form of plasticity induced in rat barrel cortex. Somatosens Mot Res. 16:122-138. (Pubitemid 29352197)
76. Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, Huntley GW. 2008. Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci U S A. 105:19520-19525.
77. Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, Wawrzyniak M, Malinowska M, Okulski P, Kolodziej LR, et al. 2008. Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol. 180:1021-1035. (Pubitemid 351398426)
78. Wimmer VC, Broser PJ, Kuner T, Bruno RM. 2010. Experience-induced plasticity of thalamocortical axons in both juveniles and adults. J Comp Neurol. 518:4629-4648.
79. Wirtshafter D. 2005. Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment. Brain Res. 1051:57-65. (Pubitemid 40982626)