Increased interaction of dopamine-immunoreactive varicosities with GABA neurons of rat medial prefrontal cortex occurs during the postweanling period

Synapse

Volumn 23, Issue 4, 1996, Pages 237-245

  Benes, Francine M ^a,b   Vincent, Stephen L ^a,b   Molloy, Raymond ^b   Khan, Yusuf ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MCLEAN HOSPITAL   (United States)

Author keywords

Development; Dopamine; GABA; Medial prefrontal cortex; Nonpyramidal cells; Pyramidal cells

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; DOPAMINE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; INTERNEURON; MALE; NERVE PROJECTION; NEWBORN; NONHUMAN; PERIKARYON; POSTNATAL DEVELOPMENT; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; WEANING;

ANIMALS; DOPAMINE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA-AMINOBUTYRIC ACID; IMMUNOENZYME TECHNIQUES; MALE; NEURONS; PREFRONTAL CORTEX; RATS; VARICOSE VEINS; WEANING;

EID: 0029832669     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2396(199608)23:4<237::AID-SYN1>3.0.CO;2-8     Document Type: Article

References (63)

1. Abercrombie, M. (1946) Estimation of nuclear population from microtomic sections. Anatomic Rev., 94:239.
2. Beaudet, A., and Descarries, L. (1978) The monoamine innervation of rat cerebral cortex: Synaptic and nonsynaptic axon terminais. Neuroscience, 3:851-860.
3. Beaudet, A., and Descarries, L. (1984) Fine structure of monoamine axon terminals in cerebral cortex. In: Monoamine Innervation of Cerebral Cortex. L. Descarries, T.R. Reader, and H.H. Jasper, eds. Alan R. Liss, Inc., New York, pp. 77-94.
4. Benes, F.M. (1989) Myelination of cortical-hippocampal relays during late adolescence: Anatomical correlates to the onset of schizophrenia. Schiz. Bull., 15:585-594.
5. Benes, F.M. (1993) The relationship of cingulate cortex to schizophrenia. In: Neurobiology of Cingulate Cortex and Limbic Thalamus. B.A. Vogt, and M. Gabriel, eds. Birkhäuser, Inc., Boston, pp. 581-605.
6. Benes, F.M. (1995) Is there a neuroanatomic basis for schizophrenia? The Neuroscientist, 1:112-120.
7. Benes, F.M., McSparren, J., Bird, E.D., Vincent, S.L., and SanGiovanni, JP. (1991) Deficits in small interneurons in prefrontal and anterior cingulate cortex of schizophrenic and schizoaffective patients. Arch. Gen. Psychiat., 48:996-1001.
8. Benes, F.M., Vincent, S.L., Alsterberg, G., Bird, E.D., and SanGiovanni, J.P. (1992) Increased GABA-A receptor binding in superficial layers of cingulate cortex in schizophrenics. J. Neurosci., 12: 924-929.
9. Benes, F.M., Vincent, S.L., and Molloy, R. (1993) Dopamine-immunoreactive axon varicosities form nonrandom contacts with GABA-immunoreactive neurons in rat medial prefrontal cortex. Synapse, 15:285-295.
10. Benes, F.M., Turtle, M., Khan, Y., and Farol, P. (1994) Myelination of a key relay zone in the hippocampal formation occurs in human brain during childhood, adolescence and adulthood. Arch. Gen. Psychiat., 51:477-484.
11. Berger, B., and Verney, C. (1984) Development of the catecholamine innervation in rat neocortex. Morphological features. In: Monoamine Innervation of Cerebral Cortex. L. Descarries, T.R. Reader, and H.H. Jasper, eds. Alan R. Liss, New York, pp. 95-121.
12. Brozoski, T., Brown, R.M., Rosvold, H.E., and Goldman, P.S. (1979) Cognitive deficit caused by depletion of dopamine in prefrontal cortex of rhesus monkey. Science, 205:929-931.
13. Bruinink, A., Lichtensteiner, W., and Schlumpf, M. (1983) Pre- and postnatal ontogeny and characterization of dopaminergic D2, serotonergic S2, and spirodecanone binding sites in rat forebrain. J. Neurochem., 40:1227-1237.
14. Bunney, B.S., and Chiodo, L.A. (1984) Mesocortical dopamine systems: Further electrophysiological and pharmacological characteristics. In: Monoamine Innervation of Cerebral Cortex. L. Descarries, T.A. Reader, and H.H. Jasper, eds. Alan R. Liss, Inc., New York, pp. 263-277.
15. Carlsson, A. (1978a) Does dopamine have a role in schizophrenia? Biol. Psychiatry, 135:3-21.
16. Carlsson, A. (1978b) Antipsychotic drugs, neurotransmitters, and schizophrenia. Am. J. Psychiatry, 13:164-173.
17. Chronwall, B., and Wolff, J.R. (1980) Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J. Comp. Neurol., 190:187-208.
18. Coyle, J. T., and Enna, S. (1976) Neurochemical aspects of the ontogenesis of GABAnergic neurons in the rat brain. Brain Res., 111: 119-133.
19. Deskin, R., Seidler, F.J., Whitmore, W.L., and Slotkin, T.A. (1981) Development of a-noradrenergic and dopaminergic receptor systems depends on maturation of their presynaptic nerve terminals in the rat brain. J. Neurochem., 36:1683-1690.
20. Deutch, A. Y., and Roth, R.H. (1990) The determinants of stress-induced activation of the prefrontal cortical dopamine system. Prog. Brain Res., 85:367-403.
21. Deutch, A. Y., Gruen, R.J., and Roth, R.H. (1989) The effects of perinatal diazepam exposure on stress-induced activation of the mesotelencephalic dopamine system. Neuropsychopharmacology 2:105-114.
22. Flechsig, P. (1920) Anatomie Des Menschlichen Gehirns und Ruckenmarks auf Myelogenetischer Gundlange G. Thieme, Leipzig.
23. Gambarana, C., Pittman, R., and Siegel, R.E. (1990) Development expression of the GABA-A receptor g1 subunit mRNA in the rat brain. J. Neurobiol., 21:1169-1179.
24. Geffard, M., Buijs, R.M., Sequela, P., Pool, C.W., and Le Moal, M. (1984) First demonstration of highly specific and sensitive antibodies against dopamine. Brain Res., 294:161-165.
25. Gellman, R.L., and Aghajanian, G.K. (1993) Pyramidal cells in piriform cortex receive a convergence of inputs from monoamine activated GABAergic interneurons. Brain Res., 600:63-73.
26. Goldman-Rakic, P.S., Leranth, C., William, S.M., Mons, N., and Geffard, M. (1989) Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc. Natl. Acad. Sci. U.S.A., 86:9015-9019.
27. Johnston, M.V. (1988) Biochemistry of neurotransmitters in cortical development. In: Cerebral Cortex. A. Peter, and E.G. Jones, eds. Plenum Press, New York, pp. 211-236.
28. Kalsbeek, A., Voorn, P., Buijs, R.M., Pool, C.W., and Uylings, H.B. (1988) Development of the dopaminergic innervation in the prefrontal cortex of rat. J. Comp. Neurol., 269:58-72.
29. Kraepelin, E. (1919) Dementia Praecox and Paraphrenia. E. and S. Livingston, Edinburg.
30. Lavielle, S., Tassin, J.P., Thierry, A.M., Blanc, G., Herve, D., Barthelemy, C., and Glowinski, J. (1978) Blockade by benzodiazepines of the selective high increase in dopamine turnover by stress in mesocortical dopaminergic neurons of the rat. Brain Res., 168:585-594.
31. Lindvall, O., and Bjorklund, A. (1978) Anatomy of the dopaminergic neuron systems in the rat brain. In: Advances in Biochemical Psychopharmacology. P.J. Roberts, e.al., eds. Raven Press, New York, pp. 1-23.
32. Lindvall, O., and Bjorkland, A. (1984) General organization of cortical monoamine systems. In: Monoamine Innervation of Cerebral Cortex. Descarries, L., Reader, T.R., and Jasper, H.H., Eds. Alan R. Liss, New York, pp. 9-40.
33. Luhmann, H.J., and Prince, D.A. (1991) Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol., 65:247-263.
34. Meltzer, H.Y., and Stahl, S.M. (1976) The dopamine hypothesis of schizophrenia: A review. Schiz. Bull., 2:19-76.
35. Morilak, D.A., Garlow, S.J., and Ciaranello, R.D. (1993) Immunocytochemical localization and description of neurons expressing 5-HT-2 receptors in the rat brain. Neuroscience, 54:701-717.
36. Palacios, J.M., Niehoff, D.L., and Kuhar, M.J. (1979) Ontogeny of GABA and benzodiazepine receptors: Effects of Triton X-100, bromide and muscimol. Brain Res., 179:390-395.
37. Palmer, M.R., and Hoffer, B.J. (1980) Catecholamine modulation of enkephalin-induced electrophysiological responses in cerebral cortex. J. Pharmacol. Exp. Ther., 213:205-215.
38. Parnavelas, J.G., Papadopoulos, G.C., and Cavanagh, M.E. (1988) Changes in neurotransmitters during development. In: Cerebral Cortex. A. Peters, and E.G. Jones, eds. Plenum Press, New York, pp. 177-209.
39. Penit-Soria, J., Audinat, E., and Crepel, F. (1987) Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiolgoical study. Brain Res., 425:363-374.
40. Reader, T.A., Ferron, A., Descarries, L. and Jasper, H.H. (1979) Modulatory role for biogenic amines in the cerebral cortex. Microiontophoretic studies. Brain Res., 160:217-229.
41. Retaux, S., Besson, M.J., and Penit-Soria, J. (1991a) Opposing effects of dopamine D2 receptor stimulation on the spontaneous and the electrically evoked release of [3H]GABA on rat prefrontal cortex slices. Neuroscience, 42:61-71.
42. Retaux, S., Besson, M.J., and Penit-Soria, J. (1991b) Synergism between D1 and D2 dopamine receptors in the inhibition of the evoked release of [3H]GABA in the rat prefrontal cortex. Neuroscience, 43:323-329.
43. Reynolds, G.P., Czudek, C., and Andrews, H. (1990) Deficit and hemispheric asymmetry of GABA uptake sites in the hippocampus in schizophrenia. Biol. Psychiatry, 27:1038-1044.
44. Roberts, E. (1972) An hypothesis suggesting that there is a defect in the GABA system in schizophrenia. Neurosci. Res. Bull., 10:469-482.
45. Roth, R.H., Tam, S.Y., Ida, Y., Yang, J.X., and Deutch, A.Y. (1988) Stress and the mesocorticolimbic dopamine systems. Ann. N.Y. Acad. Sci., 537:138-147.
46. Seeman, P. (1981) Brain dopamine receptors. Pharmacol. Rev., 32: 229-313.
47. Seguela, P., Watkins, K.C., and Descarries, L. (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and suprarhinal cortex of rat. J. Comp. Neurol., 289:11-22.
48. Sheldon, P.W., and Aghajanian, G.K. (1990) Serotonin (5-HT) induces IPSPs in pyramidal layer cells of rat piriform cortex: Evidence for the involvement of a 5-HT2-activated interneuron. Brain Res., 506:62-69.
49. Sillito, A.M. (1984) Functional considerations of the operation of GABAergic inhibitory processes in the visual cortex. In: Cerebral Cortex. E.G. Jones, and A. Peters, eda. Plenum Press, New York, pp. 91-118.
50. Simpson, M.D., Slater, P., Deakin, J.F., Royston, M.C., and Skan, W.J. (1989) Reduced GABA uptake sites in the temporal lobe in schizophrenia. Neurosci. Lett., 107:211-215.
51. Spoerri, P.E. (1988) Neurotrophic effects of GABA in cultures of embryonic chick brain and retina. Synapse, 2:11-22.
52. Tam, S., and Roth, R. (1990) Modulation of mesoprefrontal dopamine neurons by central benzodiazepine receptors. I. Pharmacological characterization. J. Pharmacol. Exper. Ther., 252:989-996.
53. Taylor, J.B., and Benes, F.M. (1994) Colocalization of glutamate decarboxylase (GAD), serotonin (5HT) and tyrosine hydroxylase (TH) in rat medial prefrontal cortex (mPFC). Soc. Neurosci. Abs., 20:638.14.
54. Thierry, A.M., Tassin, J.P, Blanc, G., and Glowinski, J. (1976) Selective activation of the mesocortical DA system by stress. Nature, 263: 242-244.
55. Thierry, A.M., Mantz, J., Milla, C., and Glowinski, J. (1988) Influence of the mesocortical/prefrontal dopamine neurons on their target cells. In: The Mesocorticolimbic Dopamine System. P.W. Kalivas, and C.B. Nemeroff, eds. Ann. N.Y. Acad. Sci., 537:101-111.
56. Verney, C., Berger, B., Adrien, J., Vigny, A., and Gay, M. (1982) Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using anti-tyrosine hydroxylase antibodies. Dev. Brain Res., 5:41-52.
57. Verney, C., Alvarez, C., Gerrard, M., and Berger, B. (1990) Ultrastructural double-labelling study of dopamine terminals and GABA-containing neurons in rat anteromedial cortex. Eur. J. Neurosci., 2:960-972.
58. Vincent, S.L., Pabreza, L., and Benes, F.M. (1995) Postnatal maturation of GABA-Immunoreactive neurons of rat medial prefrontal cortex. J. Comp. Neurol., 355:81-92.
59. Vincent, S.L., Khan, Y., and Benes, F.M. (1993) Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex. J. Neurosci., 13:2551-2561.
60. Vincent, S.L., Khan, Y., and Benes, F.M. (1995) Cellular colocalization of dopamine D1 and D2 receptors in rat medial prefrontal cortex. Synapse, 19:112-120.
61. Weibel, E.R. (1979) 2. Elementary Introduction to Stereological Principles. Stereological Methods. Vol. 1 Practical Methods for Biological Morphometry. Academic Press, New York, pp. 46-57.
62. Weinberger, D.R. (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry, 44: 660-669.
63. Yakovlev, P., and Lecours, A. (1967) The myelinogenetic cycles of regional maturation of the brain. In: Regional Development of the Brain Early in Life. A. Minkowski, ed. Oxford, Blackwell, pp. 3-70.