Spatiotemporal distribution of proteoglycans in the developing rat's barrel field and the effects of early deafferentation

Journal of Comparative Neurology

Volumn 510, Issue 2, 2008, Pages 145-157

  Bahia, Carlomagno Pacheco ^a,b   Houzel, Jean Christophe ^b   Picanço Diniz, Cristovam Wanderley ^a   Pereira Jr , Antonio ^a  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Critical period; Extracellular matrix; Perineuronal net; Plasticity; Proteoglycans; Somatosensory cortex

Indexed keywords

PLANT LECTIN; PROTEOGLYCAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEAN; BIOTINYLATION; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DEAFFERENTATION; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RAT; SOMATOSENSORY CORTEX; VIBRISSA;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, NEWBORN; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHYSIOLOGY; EXTRACELLULAR MATRIX; NEURONS; PLANT LECTINS; PROTEOGLYCANS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 50249161974     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21781     Document Type: Article

References (91)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Alpar A, Gartner U, Hartig W, Bruckner G. 2006. Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat. Brain Res 1120:13-22.
3. Bender KJ, Allen CB, Bender VA, Feldman DE. 2006. Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J Neurosci 26:4155-4165.
4. Beneyto M, Rueda J, Merchan JA, Prieto JJ. 1999. Specific staining of nonpyramidal cell populations of the cerebral cortex by lectin cytochemistry on semithin sections. Brain Res Bull 49:251-262.
5. Bertolotto A, Rocca G, Schiffer D. 1990. Chondroitin 4-sulfate proteoglycan forms an extracellular network in human and rat central nervous system. J Neurol Sci 100:113-123.
6. Bruckner G, Seeger G, Brauer K, Hartig W, Kacza J, Bigl V. 1994. Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res 658:67-86.
7. Bruckner G, Hartig W, Kacza J, Seeger J, Welt K, Brauer K. 1996. Extracellular matrix organization in various regions ofrat brain grey matter. J Neurocytol 25:333-346.
8. Bruckner G, Hartig W, Seeger J, Rubsamen R, Reimer K, Brauer K. 1998. Cortical perineuronal nets in the gray short-tailed opossum (Monodelphis domestica): a distribution pattern contrasting with that shown in placental mammals. Anat Embryol (Berl) 197:249-262.
9. Bruckner G, Grosche J, Hartlage-Rubsamen M, Schmidt S, Schachner M. 2003. Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 26:37-50.
10. Bruckner G, Szeoke S, Pavlica S, Grosche J, Kacza J. 2006. Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience 138:365-375.
11. Celio MR, Blumcke I. 1994. Perineuronal nets - a specialized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19:128-145.
12. Celio MR, Chiquet-Ehrismann R. 1993. 'Perineuronal nets'around cortical interneurons expressing parvalbumin are rich in tenascin. Neurosci Lett 162:137-140.
13. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L. 1998. Perineuronal nets: past and present. Trends Neurosci 21:510-515.
14. Cohen-Tannoudji M, Babinet C, Wassef M. 1994. Early determination of a mouse somatosensory cortex marker. Nature 368:460-463.
15. Cooper NG, Steindler DA. 1986a. Monoclonal antibody to glial fibrillary acidic protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex. Brain Res 380:341-348.
16. Cooper NG, Steindler DA. 1986b. Lectins demarcate the barrel subfield in the somatosensory cortex of the early postnatal mouse. J Comp Neurol 249:157-169.
17. Daw MI, Scott HL, Isaac JT. 2007. Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Molecular and cellular neurosciences 34:493-502.
18. Dawson DR, Killackey HP. 1985. Distinguishing topography and somatotopy in the thalamocortical projections of the developing rat. Brain Res 349:309-313.
19. Dawson DR, Killackey HP. 1987. The organization and mutability of the forepaw and hindpaw representations in the somatosensory cortex of the neonatal rat. J Comp Neurol 256:246-256.
20. Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, Sugahara K, Fawcett JW. 2006. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 281:17789-17800.
21. Derouiche A, Hartig W, Brauer K, Bruckner G. 1996. Spatial relationship of lectin-labelled extracellular matrix and glutamine synthetase-immunoreactive astrocytes in rat cortical forebrain regions. J Anat 189(Pt 2):363-372.
22. Dityatev A, Schachner M. 2003. Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4:456-468.
23. Elston GN, DeFelipe J, Arellano JI, Gonzilez-Albo MC, Rosa MG. 1999. Variation in the spatial relationship between parvalbumin immunoreactive interneurones and pyramidal neurones in rat somatosensory cortex. Neuroreport 10:975-2979.
24. Faissner A, Steindler D. 1995. Boundaries and inhibitory molecules in developing neural tissues. Glia 13:233-254.
25. Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC. 2007. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56:907-923.
26. Freire MA, Gomes-Leal W, Carvalho WA, Guimaraes JS, Franca JG, Picanco-Diniz CW, Pereira A Jr. 2004. A morphometric study of the progressive changes on NADPH diaphorase activity in the developing rat's barrel field. Neurosci Res 50:55-66.
27. Fuchs JL, Salazar E. 1998. Effects of whisker trimming on GABA(A) receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol 395:209-216.
28. Fukuda T, Kosaka T, Singer W, Galuske RAW. 2006. Gap junctions among dendrites of cortical GABAergic neurons establish a dense and wide-spread intercolumnar network. J Neurosci 26:3434-3443.
29. Galtrey CM, Fawcett JW. 2007. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1-18.
30. Geisert E, Bidanset D. 1993. A central nervous system keratan sulfate proteoglycan: localization to boundaries in the neonatal rat brain. Brain Res Dev Brain Res 75:163-173.
31. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
32. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
33. Hartig W, Brauer K, Bruckner G. 1992. Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 3:869-872.
34. Hausen D, Brückner G, Drlicek M, Härtig W, Brauer K, Bigl V. 1996. Pyramidal cells ensheathed by perineuronal nets in human motor and somatosensory cortex. Neuroreport 7:1725-1729.
35. Hendry SH, Jones EG, Hockfield S, McKay RD. 1988. Neuronal populations stained with the monoclonal antibody Cat-301 in the mammalian cerebral cortex and thalamus. J Neurosci 8:518-542.
36. Herndon ME, Lander AD. 1990. A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron 4:949-961.
37. Howard CV, Reed M. 2005. Unbiased stereology: three-dimensional measurement in microscopy. Jones C, editor. New York: BIO Scientific.
38. Inan M, Crair MC. 2007. Development of cortical maps: perspectives from the barrel cortex. Neuroscientist 13:49-61.
39. Inan M, Lu H-C, Albright MJ, She W-C, Crair MC. 2006. Barrel map development relies on protein kinase a regulatory subunit IIbeta-mediated cAMP signaling. J Neurosci 26:4338-4349.
40. Innocenti GM, Price DJ. 2005. Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955-965.
41. Ivy GO, Akers RM, Killaekey HP. 1979. Differential distribution of callosal projection neurons in the neonatal and adult rat. Brain Res 173:532-537.
42. Jhaveri S, Erzurumlu RS, Crossin K. 1991. Barrel construction in rodent neocortex: role of thalamic afferents versus extracellular matrix molecules. Proc Natl Acad Sci U S A 88:4489-4493.
43. John N, Krugel H, Frischknecht R, Smalla KH, Schultz C, Kreutz MR, Gundelfinger ED, Seidenbecher CI. 2006. Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 31:774-784.
44. Kaas JH, Qi HX, Burish MJ, Gharbawie OA, Onifer SM, Massey JM. 2008. Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord. Exp Neurol 209:407-416.
45. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
46. Koppe G, Bruckner G, Brauer K, Hartig W, Bigl V. 1997. Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res 288:33-41.
47. Koralek KA, Jensen KF, Killackey HP. 1988. Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex. Brain Res 463:346-351.
48. Kosaka T, Heizmann CW. 1989. Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res 483:158-163.
49. Land PW, Simons DJ. 1985. Cytochrome oxidase staining in the rat SmI barrel cortex. J Comp Neurol 238:225-235.
50. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM. 2006. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26:4406-4414.
51. McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT. 2007. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 27:5405-5413.
52. Mulligan KA, van Brederode JF, Hendrickson AE. 1989. The lectin Vicia villosa labels a distinct subset of GABAergic cells in macaque visual cortex. Vis Neurosci 2:63-72.
53. Nakagawa F, Schulte BA, Wu SJY, Spicer S. 1986. GABAergic neurons of rodent brain correspond partially with those staining for glycoconjugate with terminal N-acetylgalactosamine. J Neurocytol 15:389-396.
54. Ohyama J, Ojima H. 1997. Labeling of pyramidal and nonpyramidal neurons with lectin Vicia villosa during postnatal development of the guinea pig. J Comp Neurol 389:453-468.
55. Ojima H, Kuroda M, Ohyama J, Kishi K. 1995. Two classes of cortical neurones labelled with Vicia villosa lectin in the guinea-pig. Neuroreport 6:617-620.
56. Olavarria J, Van Sluyters RC, Killackey HP. 1984. Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291:364-368.
57. Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda N. 1994. Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 60:145-157.
58. Pereira A Jr, Freire M-AM, Bahia CP, Franca JG, Picanco-Diniz CW. 2000. The barrel field of the adult mouse Sml cortex as revealed by NADPH-diaphorase histochemistry. Neuroreport 11:1889-1892.
59. Petersen CC. 2007. The functional organization of the barrel cortex. Neuron 56:339-355.
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.
61. Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L. 2006. Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A 103:8517-8522.
62. Rauch U. 1997. Modeling an extracellular environment for axonal path-finding and fasciculation in the central nervous system. Cell Tissue Res 290:349-356.
63. Rice FL. 1985. Gradual changes in the structure of the barrels during maturation of the primary somatosensory cortex in the rat. J Comp Neurol 236:496-503.
64. Rice F. 1995. Comparative aspects of barrel structure and development. In: Jones EG, Diamond IT, editors. The barrel cortex of rodents. New York: Plenum Press. p 1-62.
65. Rice FL, Gomez C, Barstow C, Burnet A, Sands P. 1985. A comparative analysis of the development of the primary somatosensory cortex: interspecies similarities during barrel and laminar development. J Comp Neurol 236:477-495.
66. Riggs GH, Schweitzer L. 1994. Changing patterns of peanut agglutinin labelling in the dorsal cochlear nucleus correspond to axonal ingrowth. J Anat 185(Pt 2):387-396.
67. Rosen GD, Windzio H, Galaburda AM. 2001. Unilateral induced neocortical malformation and the formation of ipsilateral and contralateral barrel fields. Neuroscience 103:931-939.
68. Ruoslahti E. 1996. Brain extracellular matrix. Glycobiology 6:489-492.
69. Schierloh A, Eder M, Zieglgansberger W, Dodt HU. 2004. Effects of sensory deprivation on columnar organization of neuronal circuits in the rat barrel cortex. Eur J Neurosci 20:1118-1124.
70. Schweizer M, Streit WJ, Muller CM. 1993. Postnatal development and localization of an N-acetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex. J Comp Neurol 329:313-327.
71. Seidenbecher CI, Richter K, Rauch U, Fassler R, Garner CC, Gundelfinger ED. 1995. Brevican, a chondroitin sulfate proteoglycan of rat brain, occurs as secreted and cell surface glycosylphosphatidylinositol- anchored isoforms. J Biol Chem 270:27206-27212.
72. Seidenbecher CI, Gundelfinger ED, Bockers TM, Trotter J, Kreutz MR. 1998. Transcripts for secreted and GPI-anchored brevican are differentially distributed in rat brain. Eur J Neurosci 10:1621-1630.
73. Shu SY, Ju G, Fan LZ. 1988. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85: 169-171.
74. Steindler DA. 1993. Glial boundaries in the developing nervous system. Annu Rev Neurosci 16:445-470.
75. Steindler DA, Cooper NG, Faissner A, Schachner M. 1989. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243-260.
76. Tollefsen SE, Kornfeld R. 1983. The B4 lectin from Vicia villosa seeds interacts with N-acetylgalactosamine residues alpha-linked to serine or threonine residues in cell surface glycoproteins. J Biol Chem 258: 5172-5176.
77. Tollefsen S, Kornfeld R. 1987. Vicia villosa lectins. Methods Enzymol 138:536-544.
78. Uziel D, Garcez P, Lent R, Peuckert C, Niehage R, Weth F, Bolz J. 2006. Connecting thalamus and cortex: the role of ephrins. Anat Rec A Discov Mol Cell Evol Biol 288:135-142.
79. Van der Loos H, Woolsey TA. 1973. Somatosensory cortex: structural alterations following early injury to sense organs. Science 179:395-398.
80. Viggiano D. 2000. The two faces of perineuronal nets. Neuroreport 11: 2087-2090.
81. Wallace MN. 1987. Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex. Brain Res 418:178-182.
82. Watanabe E, Aono S, Matsui F, Yamada Y, Naruse I, Oohira A. 1995. Distribution of a brain-specific proteoglycan, neurocan, and the corresponding mRNA during the formation of barrels in the rat somatosensory cortex. Eur J Neurosci 7:547-554.
83. Welker C. 1971. Microelectrode delineation of fine grain somatotopic organization of (SmI) cerebral neocortex in albino rat. Brain Res 26:259-275.
84. Welker C. 1976. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166:173-189.
85. Welker E, Van der Loos H. 1986. Quantitative correlation between barrel-field size and the sensory innervation of the whiskerpad: a comparative study in six strains of mice bred for different patterns of mystacial vibrissae. J Neurosci 6:3355-3373.
86. Welker C, Woolsey TA. 1974. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol 158:437-453.
87. Wintergerst ES, Faissner A, Celio MR. 1996. The proteoglycan DSD-1-PG occurs in perineuronal nets around parvalbumin-immunoreactive interneurons of the rat cerebral cortex. Int J Dev Neurosci 14:249-255.
88. Wong-Riley M. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11-28.
89. Wong-Riley M, Welt C. 1980. Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci U S A 77:2333-2337.
90. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
91. Yamaguchi Y. 2000. Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57:276-289.