Perineuronal nets ensheath fast spiking, parvalbumin-immunoreactive neurons in the medial septum/diagonal band complex

European Journal of Neuroscience

Volumn 12, Issue 3, 2000, Pages 828-838

  Morris, Neil P ^a   Henderson, Zaineb ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Adaptation; Immunofluorescence; Intracellular recording; Lectin; Rat

Indexed keywords

BIOCYTIN; LECTIN; PARVALBUMIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; ELECTROPHYSIOLOGY; EXTRACELLULAR MATRIX; GABAERGIC SYSTEM; HIPPOCAMPUS; IMMUNOREACTIVITY; LIMBIC SYSTEM; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; ANIMALS; DIAGONAL BAND OF BROCA; ELECTROPHYSIOLOGY; FEMALE; IMMUNOHISTOCHEMISTRY; LYSINE; MALE; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; NERVE NET; NEURONS; OLIGODENDROGLIA; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SEPTUM OF BRAIN;

EID: 0034084881     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00970.x     Document Type: Article

References (83)

1. Alonso, J.R., Covenas, R., Lara, J. & Aijon, J. (1990) Distribution of parvalbumin immunoreactivity in the rat septal area. Brain Res. Bull., 24, 41-48.
2. Alonso, A., Gaztelu, J.M., Buno, W. Jr & Garcia-Austt, E. (1987) Cross-correlation analysis of septohippocampal neurons during theta rhythm. Brain Res., 413, 135-146.
3. Bertolotto, A., Manzardo, E. & Guglielmone, R. (1996) Immunohistochemical mapping of perineuronal nets containing chondroitin unsulfated proteoglycan in the rat central nervous system. Cell Tiss. Res., 283, 283-295.
4. Bignami, A., Asher, R. & Perides, G. (1992) Co-localisation of hyaluronic acid and chondroitin sulfate proteoglycan in rat cerebral cortex. Brain Res., 579, 173-177.
5. Bignami, A., Dahl, D., Gilad, V.H. & Gilad, G.M. (1988) Hyaluronate-binding protein produced by white matter astrocyles: an axonal growth repellent? Exp. Neurol., 100, 253-256.
6. Bilkey, D.K. & Goddard, G.V. (1987) Septohippocampal and commissural pathways antagonistically control inhibitory interneurons in the dentate gyrus. Brain Res., 405, 320-325.
7. Brauer, K., Hanig, W., Bigl, V. & Bruckner, G. (1993) Distribution of parvalbumin-containing neurons and lectin-binding perineuronal nets in the rat basal forebrain. Brain Res., 631, 167-170.
8. Bruckner, G., Brauer, K., Hartig, W., Wolff, J.R., Rickmann, M.J., Derouiche, A., Delpech, B., Girard, N., Oertel, W.H. & Reichenbach, A. (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia, 8, 183-200.
9. Bruckner, G., Schutz, A., Hartig, W., Brauer, K., Paulke, B.R. & Bigl, V. (1994a) Projection of non-cholinergic basal forebrain neurons ensheathed with perineuronal nets to rat mesocortex. J. Chem. Neuroanat., 8, 11-18.
10. Bruckner, G., Seeger, G., Brauer, K., Hartig, W., Kacza, J. & Bigl, V. (1994b) Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res., 658, 67-86.
11. Cauli, B., Audinat, E., Lambolez, B., Angulo, M.C., Ropert, N., Tsuzuki, K., Hestrin, S. & Rossier, J. (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci, 17, 3894-3906.
12. Celio, M.R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science, 231, 995-997.
13. Celio, M.R. (1993) Perineuronal nets of extracellular matrix around parvalbumin-containing neurons of the hippocampus. Hippocampus, 3, 55-60.
14. Celio, M.R. & Blumcke, I. (1994) Perineuronal nets - a specialised form of extracellular matrix in the adult nervous system. Brain Res. Rev., 19, 128-145.
15. Celio, M.R. & Chiquet-Ehrismann, R. (1993) 'Perineuronal nets' around cortical interneurons expressing parvalbumin are rich in tenascin. Neurosci. Lett., 162, 137-140.
16. Chen, W., Zhang, J.J., Hu, G.Y. & Wu, C.P. (1996b) Different mechanisms underlying the repolarisation of narrow and wide action potentials in pyramidal cells and interneurons of cat motor cortex. Neuroscience, 73, 57-68.
17. Choi, D.W. & Rothman, S.M. (1990) The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci., 13, 171-182.
18. Detari, L. & Vanderwolf, C.H. (1987) Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetised rats. Brain Res., 437, 1-8.
19. Drake, C.T., Mulligan, K.A., Wimpey, T.L., Hendrickson, A. & Chavkin, C. (1991) Characterisation of Vicia villosa agglutinin-labelled GABAergic interneurons in the hippocampal formation and in acutely dissociated hippocampus. Brain Res., 554, 176-185.
20. Du, J., Zhang, L., Weiser, M., Rudy, B. & McBain, C.J. (1996) Developmental expression and functional characterisation of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci, 16, 506-518.
21. Dutar, P., Bassant, M.H., Senut, M.C. & Lamour, Y. (1995) The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev., 75, 393-427.
22. Dutar, P., Lamour, Y., Rascol, O. & Jobert, A. (1986) Septo-hippocampal neurons in the rat - further study of their physiological and pharmacological properties. Brain Res., 365, 325-334.
23. Everitt, B.J. & Robbins, T.W. (1997) Central cholinergic systems and cognition. Annu. Rev. Psychol., 48, 649-684.
24. Ford, R.D., Colom, L.V. & Bland, B.H. (1989) The classification of medial septum-diagonal band cells as theta-on or theta-off in relation to hippocampal EEG states. Brain Res., 493, 269-282.
25. Freund, T.F. (1989) GABAergic septohippocampal neurons contain parvalbumin. Brain Res., 478, 375-381.
26. Freund, T.F. & Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336, 170-173.
27. Gallo, V. & Bertolotto, A. (1990) Extracellular matrix of cultured glial cells: selective expression of chondroitin 4-sulfate by type-2 astrocytes and their progenitors. Exp. Cell Res., 187, 211-223.
28. Gogolak, G., Petsche, H., Stere, J. & Stumpf, C. (1967) Septum cell activity in the rabbit under reticular stimulation. Brain Res., 5, 508-510.
29. Gorelova, N. & Reiner, P.B. (1996) Role of the afterhyperpolarisation in control of discharge properties of septal cholinergic neurons in vitro. J. Neurophysiol, 75, 695-706.
30. Griffith, W.H. (1988) Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J. Neurophysiol., 59, 1590-1612.
31. Griffith, W.H. & Matthews, R.T. (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci. Lett., 71, 169-174.
32. Griffith, W.H., Sim, J.A. & Matthews, R.T. (1991) Electrophysiological characteristics of basal forebrain neurons in vitro. Adv. Exp. Med. Biol., 295, 143-155.
33. Griffith, W.H., Taylor, L. & Davis, M.J. (1994) Whole-cell and single-channel calcium currents in guinea pig basal forebrain neurons. J. Neurophysiol., 71, 2359-2376.
34. Gritti, I., Mainville, L. & Jones, B.E. (1993) Codistribution of GABA-with acetylcholine-synthesising neurons in the basal forebrain of the rat. J. Camp. Neurol., 329, 438-457.
35. Gulyas, A.I., Gores, T.J. & Freund, T.F. (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience, 37, 31-44.
36. Hartig, W., Brauer, K., Bigi, V. & Bruckner, G. (1994) Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labelled perineuronal nets around parvalbumin-containing neurons. Brain Res., 635, 307-311.
37. Hartig, W., Brauer, K. & Bruckner, G. (1992) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport, 3, 869-872.
38. Hartig, W., Bruckner, G., Brauer, K., Schmidt, C. & Bigl, V. (1995) Allocation of perineuronal nets and parvalbumin-immunoreactivity, calbindin-D28k-immunoreactivity and glutamic-acid decarboxylase-immunoreactivity in the amygdala of the rhesus-monkey. Brain Res., 698, 265-269.
39. Houser, C.R., Vaughn, J.E., Hendry, S.H.C., Jones, E.G. & Peters, A. (1984) GABA neurons in the cerebral cortex. In Jones, E.G., Peters, A., (eds), Functional Properties of Cortical Cells. Plenum Press, New York. pp. 63-89.
40. Jakab, R.L. & Leranth, C. (1995) Septum. In Paxinos, G. (ed), The Rat Nervous System, Vol. 2, Academic Press, London, pp. 405-441.
41. Johnson-Green, P.C., Dow, K.E. & Riopelle, R.J. (1991) Characterisation of glycosaminoglycans produced by primary astrocytes in vitro. Glia, 4, 314-321.
42. Kawaguchi, Y. (1993) Physiological, morphological and histochemical characterisation of three classes of interneurons in rat neostriatum. J. Neurosci, 13, 4908-4923.
43. Kawaguchi, Y. (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci, 15, 2638-2655.
44. Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C.W. & Hama, K. (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res., 416, 369-374.
45. Kawaguchi, Y. & Kubota, Y. (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin-and calbindin D28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol., 70, 387-396.
46. Kawaguchi, Y. & Kubola, Y. (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex, 7, 476-486.
47. Kiss, J., Patel, A.J., Baimbridge, K.G. & Freund, T.F. (1990a) Topographical localisation of neurons containing parvalbumin and choline acetyltransferase in the medial septum-diagonal band region of the rat. Neuroscience, 36, 61-72.
48. Kiss, J., Patel, A.J. & Freund, T.F. (1990b) Distribution of septohippocampal neurons containing parvalbumin or choline acetyltransferase in the rat brain. J. Comp. Neurol., 298, 362-372.
49. Kita, H., Kosaka, T. & Heizmann, C.W. (1990) Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res., 536, 1-15.
50. Kobayashi, K., Emson, P.C. & Mountjoy, C.Q. (1989) Vicia villosa lectin-positive neurones in human cerebral cortex. Loss in Alzheimer-type dementia. Brain Res., 498, 170-174.
51. Kohler, C., Chan-Palay, V. & Wu, J. (1984) Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anal. Embryol., 169, 41-44.
52. Kosaka, T. & Heizmann, C.W. (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.
53. Kosaka, T., Heizmann, C.W. & Barnstable, C.J. (1989) Monoclonal antibody VC1.1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp. Brain Res., 78, 43-50.
54. Kubota, Y. & Kawaguchi, Y. (1994) Three classes of GABAergic interneurons in neocortex and neostriatum. Jpn. J. Physiol., 44, 145-148.
55. Lafarga, M., Berciano, M.T. & Blanco, M. (1984) The perineuronal net in the fastigial nucleus of the rat cerebellum. A Golgi and quantitative study. Anat. Embryol., 170, 79-85.
56. Lamour, Y., Dutar, P. & Jobert, A. (1984) Septo-hippocampal and other medial septum-diagonal band neurons: electrophysiological and pharmacological properties. Brain Res., 309, 227-239.
57. Lee, M.G., Chrobak, J.J., Sik, A., Wiley, R.G. & Buzsaki, G. (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience, 62, 1033-1047.
58. Lenz, S., Perney, T.M., Qin, Y., Robbins, E. & Chesselet, M.F. (1994) GABAergic interneurons of the striatum express the shaw-like potassium channel Kv3.1. Synapse, 18, 55-66.
59. Locke, R.E. & Nerbonne, J.M. (1997) Role uf voltage-gated K+ currents in mediating the regular-spiking phenotype of callosal-projecting rat visual cortical neurons. J. Neurophysiol., 78, 2321-2335.
60. Luth, H.J., Fischer, J. & Celio, M.R. (1992) Soybean lectin binding neurons in the visual cortex of the rat contain parvalbumin and are covered by glial nets. J. Neurocytol., 21, 211-221.
61. Markram, H. & Segal, M. (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res., 513, 171-174.
62. Morris, N.P., Harris, S.J. & Henderson, Z. (1999) Parvalbumin-immunoreactive, fast-spiking neurons in the medial septum/diagonal band complex of the rat: intracellular recordings in vitro. Neuroscience, 92, 589-600.
63. Mugnaini, E. & Oertal, W.H. (1985) An Atlas of the Distribution of Gabaergic Neurons and Terminals in the Rat CNS as Revealed by GAD Immunohistochemistry. In Bjorklund, A., Hokfelt, T., (eds), GABA and neuropeptides in the CNS. Elsevier, Amsterdam, pp. 436-608.
64. Naegele, J.R., Arimatsu, Y., Schwanz, P. & Barnstable, C.J. (1988) Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC·1.1. J. Neurosci, 8, 79-89.
65. Naegele, J.R. & Katz, L.C. (1990) Cell surface molecules containing N-acetylgalactosamine are associated with basket cells and neurogliaform cells in cat visual cortex. J. Neurosci, 10, 540-557.
66. Nakagawa, F., Schulte, B.A., Wu, J.Y. & Spicer, S.S. (1986) GABAergic neurons of rodent brain correspond partially with those staining for glycoconjugate with terminal N-acetylgalactosamine. J. Neurocytol., 15, 389-396.
67. Paxinos, G. & Watson, C. (1996) The Rat Brain in Stereotaxic Coordinates. Academic Press Ltd, London.
68. Petsche, H., Stumpf, C. & Gogolak, G. (1962) The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. Electroencephalogr. Clin. Neurophysiol., 14, 202-211.
69. Rossner, S., Hartig, W., Schliebs, R., Bruckner, G., Brauer, K., Perez-Polo, J.R., Wiley, R.G. & Bigl, V. (1995) 192 IgG-saporin immunotoxin-induced loss of cholinergic cells differentially activates microglia in rat basal forebrain nuclei. J. Neurosci. Res., 41, 335-346.
70. Schweizer, M., Streit, W.J. & Muller, C.M. (1993) Postnatal development and localisation of an N-acetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex. J. Comp. Neurol., 329, 313-327.
71. Seeger, G., Brauer, K., Hartig, W. & Bruckner, G. (1994) Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry. Neuroscience, 58, 371-388.
72. Seeger, G., Luth, H.J., Winkelmann, E. & Brauer, K. (1996) Distribution patterns of Wisteria floribunda agglutinin binding-sites and parvalbumin-immunoreactive neurons in the human visual-cortex - a double-labelling study. J. Hirnforsch., 37, 351-366.
73. Segal, M. (1986) Properties of rat medial septal neurones recorded in vitro. J. Physiol. (Lond.), 379, 309-330.
74. Sekirnjak, C., Martone, M.E., Weiser, M., Deerinck, T., Bueno, E., Rudy, B. & Ellisman, M. (1997) Subcellular localisation of the K+ channel subunit Kv3.1b in selected rat CNS neurons. Brain Res., 766, 173-187.
75. Smythe, J.W., Colom, L.V. & Bland, B.H. (1992) The extrinsic modulation of hippocampal theta depends on the coactivation of cholinergic and GABAergic medial septal inputs. Neurosci. Biobehav. Rev., 16, 289-308.
76. Stewart, M. & Fox, S.E. (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci., 13, 163-168.
77. Sweeney, J.E., Lamour, Y. & Bassant, M.H. (1992) Arousal-dependent properties of medial septal neurons in the unanesthetised rat. Neuroscience, 48, 353-362.
78. Vertes, R.P. & Kocsis, B. (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience, 81, 893-926.
79. Vinogradova, O.S. (1995) Expression, control, and probable functional significance of the neuronal theta rhythm. Prog. Neurobiol., 45, 523-583.
80. Wainer, B.H., Levey, A.I., Rye, D.B., Mesulam, M.M. & Mufson, E.J. (1985) Cholinergic and non-cholinergic septo-hippocampal pathways. Neurosci. Lett., 54, 45-52.
81. Wintergerst, E.S., Faissner, A. & Celio, M.R. (1996) The proteoglycan DSD-1-PG occurs in perineuronal nets around parvalbumin-immunoreactive interneurons of the rat cerebral-cortex. Int. J. Devel. Neurosci., 14, 249-255.
82. Yasuhara, O., Akiyama, H., McGeer, E.G. & McGeer, P.L. (1994) Immunohistochemical localisation of hyaluronic acid in rat and human brain. Brain Res., 635, 269-282.
83. Zaremba, S., Naegele, J.R., Barnstable, C.J. & Hockfield, S. (1990) Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VC1.1. J. Neurosci, 10, 2985-2995.