Effects of monoamine oxidase a inhibition on barrel formation in the mouse somatosensory cortex: Determination of a sensitive developmental period

Journal of Comparative Neurology

Volumn 393, Issue 2, 1998, Pages 169-184

  Vitalis, Tania ^a,c   Cases, Olivier ^a,b,c   Callebert, Jacques ^d   Launay, Jean Marie ^d   Price, David J ^c   Seif, Isabelle ^b   Gaspar, Patricia ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CNRS   (France)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d HÔPITAL LARIBOISIÈRE   (France)

Author keywords

Barrels; Cerebral cortex; Clorgyline; Serotonin; Thalamocortical axons

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; ENZYME INACTIVATION; GENE EXPRESSION REGULATION; MOUSE; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL; SOMATOSENSORY CORTEX; THALAMOCORTICAL TRACT; VIBRISSA;

ANIMALS; AXONS; BEHAVIOR, ANIMAL; CLORGYLINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; HYDROXYINDOLEACETIC ACID; MICE; MONOAMINE OXIDASE INHIBITORS; PREGNANCY; SEROTONIN; SOMATOSENSORY CORTEX; THALAMUS; VIBRISSAE;

EID: 0031889318     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980406)393:2<169::AID-CNE3>3.0.CO;2-0     Document Type: Article

References (72)

1. Agmon, A., L.T. Yang, D.K. O'Dowd, and E.G. Jones (1993) Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J. Neurosci. 13:5365-5382.
2. Belford, G.R. and H.P. Killackey (1980) The sensitive period in the development of the trigeminal system of the neonatal rat. J. Comp. Neurol. 193:335-350.
3. Bennett-Clarke, C.A., M.J. Leslie, N.L. Chiaia, and R.W. Rhoades (1993) Serotonin 1B receptors in the developing somatosensory and visual cortices are located on thalamocortical axons. Proc. Natl. Acad. Sci. USA 90:153-157.
4. Bennett-Clarke, C.A., M.J. Leslie, R.D. Lane, and R.W. Rhoades (1994) Effect of serotonin depletion on vibrissa-related patterns of thalamic afferents in the rat's somatosensory system. J. Neurosci. 14:7594-7607.
5. Bennett-Clarke, C.A., R.D. Lane, and R.W. Rhoades (1995) Fenfluramine depletes serotonin from the developing cortex and alters thalamocortical organization. Brain Res. 702:255-260.
6. Blue, M.E., R.S. Erzurumlu, and S. Jhaveri (1991) A comparison of pattern formation by thalamocortical and serotonergic afferents in the rat barrel field cortex. Cerebral Cortex 1:380-389.
7. Bourgoin, S., F. Artaud, J. Adrien, F. Hery, J. Glowinski, and M. Hamon (1977) 5-Hydroxytryptamine catabolism in the rat brain during ontogenesis. J. Neurochem. 28:415-422.
8. Cases, O., I. Seif, J. Grimsby, P. Gaspar, K. Chen, S. Pournin, U. Müller, M. Aguet, C. Babinet, J.C. Shih, and E. De Maeyer (1995) Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268:1763-1766.
9. Cases, O., T. Vitalis, I. Seif, E. De Maeyer, C. Sotelo, and P. Gaspar (1996) Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: Role of a serotonin excess during the critical period. Neuron 16:297-307.
10. Catalano, S.M., R.T. Robertson, and H.P. Killackey (1996) Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J. Comp. Neurol. 367:36-53.
11. Chiaia, N.L., S.E. Fish, W.R. Bauer, C.A. Bennett-Clarke, and R.W. Rhoades (1992) Postnatal blockade of cortical activity by tetrodotoxin does not disrupt the formation of vibrissae-related patterns in the rat's somatosensory cortex. Dev. Brain Res. 66:244-250.
12. Chiaia, N.L., S.E. Fish, W.R. Bauer, B.A. Figley, M. Eck, C.A. Bennett-Clarke, and R.W. Rhoades (1994) Effects of postnatal blockade of crtical activity with tetrodotoxin upon lesion-induced reorganization of vibrissae-related patterns in the somatosensory cortex of the rat. Dev. Brain Res. 79:301-306.
13. Chiaia, N.L., C.A. Bennett-Clarke, R.S. Crissman, L. Zheng, M. Chen, and R.W. Rhoades (1996) Effect of neonatal axoplasmic transport attenuation in the infraorbital nerve on vibrissae-related patterns in the rat's brainstem, thalamus and cortex. Eur. J. Neurosci. 8:1601-1612.
14. Consolazione, A., C. Milstein, B. Wright, and A.C. Cuello (1981) Immunocytochemical detection of serotonin with monoclonal antibodies. J. Histochem. Cytochem. 29:1425-1430.
15. D'Amato, R., M.E. Blue, B.L. Largent, D.R. Lynch, D.J. Ledbetter, M.E. Molliver, and S.H. Snyder (1987) Ontogeny of the serotonergic projection to rat neocortex: Transient expression of a dense innervation to primary sensory areas. Proc. Natl. Acad. Sci. USA 84:4322-4326.
16. Daszuta, A. and P. Portalier (1985) Distribution and quantification of 5-HT nerve cell bodies in the nucleus raphe dorsalis area of C57BL and BALBc mice. Relationship between anatomy and biochemistry. Brain Res. 360:58-64
17. Daszuta, A., F. Hery, and M. Faudon (1984) In vitro 3H-serotonin (5-HT) synthesis and release in BALBc and C57BL mice. I. Terminal areas. Brain Res. Bull. 12:559-563.
18. Durham, D. and T.A. Woolsey (1984) Effects of neonatal lesions on mouse central trigeminal pathways. J. Comp. Neurol. 223:424-447.
19. Erzurumlu, R.S. and H.P. Killackey (1983) Development of order in the rat trigeminal system. J. Comp. Neurol. 213:365-380.
20. Fox, K. (1992) A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J. Neurosci. 12:1826-1838.
21. Fox, K., B.L. Schlaggar, S. Glazewski, and D.D.M. O'Leary (1996) Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex. Proc. Natl. Acad. Sci. USA 93:5584-5589.
22. Fujimiya, M., H. Kimura, and T. Maeda (1986) Postnatal development of serotonin nerve fibers in the somatosensory cortex of mice studied by immunohistochemistry. J. Comp. Neurol. 246:191-201.
23. Green, A.R. and M.B.H. Youdim (1975) Effects of monoamine oxidase inhibition by clorgyline, deprenyl or tranylcypromine on 5-hydroxytryptamine concentrations in rat brain and hyperactivity following subsequent tryptophan administration. Br. J. Pharmacol. 55:415-422.
24. Henderson, T.A., T.A. Woolsey, and M.F. Jacquin (1992) Infraorbital nerve blockade from birth does not disrupt central trigeminal pattern formation in the rat. Dev. Brain Res. 66:146-152.
25. Iwasato, T., D.F. Chen, R.S. Erzurumlu, T. Sasaoka, and S. Tonegawa (1996) Disruption of whisker-specific patterns in the somatosensory cortex and subcortical areas of the rescued NMDAR1 knockout mice. Soc. Neurosci. Abstr. 22:725.
26. Jahng, J.W., T.A. Houpt, T.C. Wessel, K. Chen, J.C. Shih, and T.H. Joh (1997) Localization of monoamine oxidase A and B mRNA in the rat brain by in situ hybridization. Synapse 25:30-36
27. Jeanmonod, D., F.L. Rice, and H. Van der Loos (1981) Mouse somatosensory cortex: Alterations in the barrelfield following receptor injury at different early postnatal ages. Neuroscience 6:1503-1535.
28. Jensen, K.F. and H.P. Killackey (1987a) Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J. Neurosci. 7:3529-3543.
29. Jensen, K.F. and H.P. Killackey (1987b) Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. II. The altered morphology of thalamocortical afferents following neonatal infraorbital nerve cut. J. Neurosci. 7:3544-3553.
30. Jourdikian, F., B. Tabakoff, and S.G.A. Alivisatos (1975) Ontogeny of multiple forms of monoamine oxidase in mouse brain. Brain Res. 93:301-308.
31. Kema, I.P., A.M. Schellings, C.J. Hoppenbrouwers, H.M. Rutgers, E.G.E. de Vries, and F.A.J. Muskiet (1993) High performance liquid Chromatographic profiling of tryptophan and related indoles in body fluids and tissues of carcinoid patients. Clin. Chim. Acta 221:143-158.
32. Killackey, H.P., N.L. Chiaia, C.A. Bennett-Clarke, M. Eck, and R.W. Rhoades (1994) Peripheral influences on the size and organization of somatotopic representations in the fetal rat cortex. J. Neurosci. 14:1496-1506.
33. Knapp, S., A.J. Mandell, P.V. Russo, A. Vitto, and K.D. Stewart (1981) Strain differences in kinetic and thermal stability of two mouse brain tryptophan hydroxylase activities. Brain Res. 230:317-336.
34. Kulikov, A.V., E.Y. Kozlachkova, N.N. Kudryavstseva, and N.K. Popova (1995) Correlation between tryptophan hydroxylase activity in the brain and predisposition to pinch-induced catalepsy in mice. Pharmacol. Biochem. Behav. 50:431-435.
35. Lebrand, C., O. Cases, C. Aldebrecht, A. Doye, C. Alvarez, S. El-Mestikawy, I. Seif, and P. Gaspar (1996) Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 77:823-835.
36. Li, Y., R.S. Erzurumlu, C. Chen, S. Jhaveri, and S. Tonegawa (1994) Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76:427-437.
37. Luque, J.M., S.W. Kwan, C.W. Abell, M. Da Prada, and J.D. Richards (1995) Cellular expression of mRNAs encoding monoamine oxidases A and B in the rat central nervous system. J. Comp. Neurol. 363:665-680.
38. Maitre, L., A. Delini-Stula, and P.C. Waldemeier (1976) Relations between the degree of monoamine oxidase inhibition and some psychopharmacological responses to monoamine oxidase inhibitors in rat. In Monoamine Oxidase and its Inhibition, Ciba Foundation Symposium 39. Amsterdam: Elsevier, pp. 247-267.
39. Mantle, T.J., N.J. Garret, and K.F. Tipton (1976) The development of monoamine oxidase in rat liver and brain. FEBS Lett. 64:227-230.
40. McCandlish, C., R.S. Waters, and N.G. Cooper (1989) Early development of the representation of the body surface in SI cortex barrel field in neonatal rats as demonstrated with peanut agglutinin binding: Evidence for differential development within the rat tunculus. Exp. Brain Res. 77:425-431.
41. Molnar, Z. and C. Blakemore (1995) How do thalamic axons find their way to the cortex? Trends Neurosci. 9:389-396.
42. Nelson, D.L., A. Herbert, J. Glowinski, and M. Hamon (1979) [3H]harmaline as a specific ligand of MAOA. II. Measurement of the rates of MAO A during ontogenesis in the rat brain. J. Neurochem. 32:1829-1836.
43. Osterheld-Haas, M.C. and J.P. Hornung (1996) Laminar development of the mouse barrel cortex: Effects of neurotoxins against monoamines. Exp. Brain Res. 110:183-195.
44. Osterheld-Haas, M.C., H. Van der Loos, and J.P. Hornung (1994) Monoaminergic afferents to cortex modulate structural plasticity in the barrelfield of the mouse. Dev. Brain Res. 77:189-202.
45. Rhoades, R.W., C.A. Bennett-Clarke, N.L. Chiaia, F.A. White, G.J. McDonald, J.H. Haring, and M.F. Jacquin (1990) Development and lesion induced reorganization of the cortical representation of the rat's body surface as revealed by immunochemistry for serotonin. J. Comp. Neurol. 293:190-207.
46. Rhoades, R.W., C.A. Bennett-Clarke, M.-Y. Shi, and R.D. Mooney (1994) Effects of 5-HT on thalamocortical synaptic transmission in the developing rat. J. Neurophysiol. 72:2438-2450.
47. Rice, F.L. and H. Van der Loos (1977) Development of the barrels and barrel field in the somatosensory cortex of the mouse. J. Comp. Neurol. 171:545-560.
48. Riddle, D., A. Richards, F. Zsuppan, and D. Purves (1992) Growth of the rat somatic sensory cortex and its constituent parts during postnatal development. J. Neurosci. 12:3509-3524.
49. Rörig, B. and B. Sutor (1996) Serotonin regulates gap junction coupling in the developing rat somatosensory cortex. Eur. J. Neurosci. 15:7386-7400.
50. Samsa, J.M., P.C. Baker, and K.M. Hoff (1979) Monoamine oxidase inhibition and recovery in the mouse brain at various ages after birth. Biol. Neonate 35:249-254.
51. Schlaggar, B.L. and D.D.M. O'Leary (1994) Early development of the somatotopic map in rat somatosensory cortex. J. Comp. Neurol. 346:80-96.
52. Senft, S.L. and T.A. Woolsey (1991a) Growth of thalamic afferents into mouse barrel cortex. Cerebral Cortex 1:308-335.
53. Senft, S.L. and T.A. Woolsey (1991b) Computer-aided analyses of thalamocortical afferent ingrowth. Cerebral Cortex 1:336-347.
54. Shatz, C.J. (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
55. Shih, J.C.(1991) Molecular basis of human MAO A and B. Neuropsychopharmacology 4:1-7.
56. Sleight, A.J., C.A. Marsden, K.F. Martin, and M.G. Palfreyman (1988) Relationship between extracellular 5-hydroxytryptamine and behaviour following monoamine oxidase inhibition and L-tryptophan. Br. J. Pharmacol. 93:303-310.
57. Stettler, O., B. Tavitian, and K.L. Moya (1996) Differential synaptic vesicle protein expression in the barrel field of developing cortex. J. Comp. Neurol. 375:321-332.
58. Tecott, L., S. Shtrom, and D. Julius (1995) Expression of a serotonin-gated ion channel in embryonic neural and nonneural tissues. Mol. Cell. Neurosci. 6:43-55.
59. Tipton, K.F. (1989) Monoamine oxidase inhibitors as antidepressants. In K.F. Tipton and M.B.H. Youdim (eds): Biochemical and Pharmacological Aspects of Depression. London: Taylor and Francis, pp. 1-24.
60. Van der Loos, H. and T.A. Woolsey (1973) Somatosensory cortex: Structural alterations following early injury to sense organs. Science 179:395-398.
61. Voitenko, N.N. (1992) Age changes in brain monoamine oxidase in mice from four lines. Voprosoy Meditsinskoi Khimii. 38:32-35.
62. Von Bartheld, C.S., M.R. Byers, R. Williams, and M. Bothwell (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379:830-833.
63. Vongdokmai, R. (1980) Effect of protein malnutrition on development of mouse cortical barrels. J. Comp. Neurol. 191:283-294.
64. Welker, E. and H. Van der Loos (1986) Quantitative correlation between barrel-field size and the sensory innervation of the whiskerpad: A comparative study of six strains of mice bred for different patterns of mystacial vibrissae. J. Neurosci. 6:3355-3373.
65. Welker, E., M. Armstrong-James, G. Bronchti, W. Ourednik, F. Gheorghita-Baechler, R. Dubois, D.L. Guernsey, H. Van der Loos, and P.E. Neumann (1996) Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless. Science 271:1864-1867.
66. Weyler, W., Y.P. Hsu, and X.O. Breakefield (1990) Biochemistry and genetics of monoamine oxidase. Pharmacol. Ther. 47:391-417.
67. Whitaker-Azmitia, P.M., X. Zhang, and C. Clarke (1994) Effects of gestational exposure to monoamine oxidase inhibitors in rats: Preliminary behavioral and neurochemical studies. Neuropsychopharmacology 11: 125-132.
68. White, E.L., L. Weinfeld, and D.L. Lev (1997) A survey of morphogenesis during the early postnatal period in PMBSF barrels of mouse Sm1 cortex with emphasis on barrel D4. Somatosens. Motor Res. 14:34-55.
69. Wilkinson, G.A., I. Farinas, C. Backus, C.K. Yoshida, and L.F. Reichardt (1997) Neurotrophin-3 is a survival factor in vivo for early mouse trigeminal neurons. J. Neurosci. 16:7661-7669.
70. Wong-Riley, M.T.T. and C. Welt (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc. Natl. Acad. Sci. USA 77:2333-2337.
71. Woolsey, T. and H. Van der Loos (1970) The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex. Brain Res. 17:205-242.
72. Woolsey, T.A. and J.R. Wann (1976) Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages. J. Comp. Neurol. 770:53-66.