Summary
The early appearance of neurotransmitters in brain tissue refers to their regulative functions on the neuronal circuits. Many neurotransmitters have direct effects on neuronal outgrowth and differentiation during brain development, which precede their role in synaptic information coding. Both the neurotrophic and neurotoxic properties of excitatory amino acids (EAAs) have focused special interest on glutamatergic neurotransmission during brain development. Therefore, this work intends to review and discuss developmental alterations of the EAA neurotransmitter system in the human brain, their relation to human brain maturation and implications for pathological processes during early human brain development.
Similar content being viewed by others
References
Arnold SE, Hyman BT, van Hoesen GW, Damasio AR (1991) Cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry 48: 625–632
Balázs R, Hack N, Jorgensen OS (1988) Stimulation of N-methyl-D-aspartate receptors has a trophic effect on differentiation of cerebellar granule cells. Neurosci Lett 87: 80–86
Barks JD, Silverstein FS, Sims K, Greenamyre JT, Johnston MV (1988) Glutamate recognition sites in human fetal brain. Neurosci Lett 84: 131–136
Beckmann H, Jakob H (1991) Prenatal disturbances of nerve cell migration in the entorhinal cortex: a common vulnerability factor in functional psychoses? J Neural Transm [Gen Sect] 84: 155–164
Becker LE, Zhang W, Pereyra PM (1993) Delayed maturation of the vagus nerve in sudden infant death syndrome. Acta Neuropathol 86: 617–622
Ben Ari Y, Cherubini E, Krnjevic K (1988) Changes in voltage dependence of NMDA currents during development. Neurosci Lett 94: 88–92
Brooksbank BWL, Martinez M, Atkinson DJ, Balazs R (1978) Biochemical development of the human brain. I. Some parameters of the cholinergic system. Dev Neurosci 1: 267–284
Butterworth J, Tennant MC (1989) Postmortem human brain pH and lactate in sudden infant death syndrome. J Neurochem 53: 1494–1499
Choi DW (1991) Excitotoxicity. In: Meldrum BS (ed) Excitatory amino acid antagonists. Blackwell Scientific Publications, Oxford, pp 216–236
Cowan WM, Fawcett JW, O'Leary DDM, Stanfield BB (1984) Regressive events in neurogenesis. Science 225: 1258–1265
Datta SC, Mukherjee KL (1983) Changes in free amino acid levels in developing human foetal brain regions. J Neurochem 40: 1150–1154
Diebler MF, Farkas-Bargeton E, Wehrle R (1979) Developmental changes of enzymes associated with energy metabolism and the synhesis of some neurotransmitters in discrete areas of human neocortex. J Neurochem 32: 429–435
Druse MJ (1992) Effects of in utero ethanol exposure on the development of neurotransmitter systems. In: Miller MW (ed) Development of the central nervous system: effects of alcohol and opiates. Wiley-Liss Inc, New York, pp 139–167
D'Souza SW, McConnell SE, Slater P, Barson AJ (1993) Glycine site of the excitatory amino acid N-methyl-D-aspartate receptor in neonatal and adult brain. Arch Dis Childhood 69: 212–215
Etienne P, Baudry M (1987) Calcium dependent aspects of synaptic plasticity, excitatory amino acid neurotransmission, brain aging and schizophrenia: a unifying hypothesis. Neurobiol Aging 8: 362–366
Farooqui AA, Horrocks LA (1991) Excitatory amino acid receptors, neural membrane phospholipid metabolism and neurological disorders. Brain Res Rev 16: 171–191
Foster AC, Wong EHF (1987) The novel anticonvulsant MK-801 binds to the activated state of the N-methyl-D-aspartate receptor in rat brain. Br J Pharmacol 91: 403–409
Gale JS (1977) Glutamic acid decarboxylase and cholineacetyltransferase in human foetal brain. Brain Res 133: 172–176
Greenamyre JT, Penney JB, Young AB, D'Amato CJ, Hicks SP, Shoulson I (1985) Alterations in glutamate binding in Alzheimer's and Huntington's disease. Science 227: 1496–1499
Greenamyre JT, Penney JB, Young AB, Hudson CH, Silverstein FS, Johnston MV (1987) Evidence for transient perinatal glutamatergic innervation of globus pallidus. J Neurosci 7: 1022–1030
Hamon B, Heinemann U (1988) Developmental changes in neuronal sensitivity to excitatory amino acids in area CA1 of the rat hippocampus. Dev Brain Res 38: 286–290
Hashimoto A, Kumashiro S, Nishikawa T, Oka T, Takahashi K, Mito T, Takashima S, Doi N, Mizutani Y, Yamazaki T, Kaneko T, Ootomo E (1993) Embryonic development and postnatal changes in free D-aspartate and D-serine in the human prefrontal cortex. J Neurochem 61: 348–351
Hashimoto A, Nishikawa T, Hayashi T, Fujii N, Harada K, Oka T, Takahashi K (1992) The presence of free D-serine in rat brain. FEBS 296: 33–36
Hebebrand J, Hofmann D, Reichelt R, Schnarr S, Knapp M, Propping P, Födisch HJ (1988) Early ontogeny of the central benzodiazepine receptor in human embryos and fetuses. Life Sci 43: 2127–2136
Hestrin S (1992) Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357: 686–689
Huttenlocher PR (1979) Synaptic density in human frontal cortex — developmental changes and effect of aging. Brain Res 163: 195–205
Huttenlocher PR, de Courten CH (1987) The development of synapses in striate cortex of man. Human Neurobiol 6: 1–9
Jakob H, Beckmann H (1986) Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J Neural Transm 65: 303–326
Johnston MV, Coyle JT (1981) Development of central neurotransmitter systems. In: The fetus and independent life. Ciba Foundation Symposium 86. Pitman, London, pp 251–270
Johnston MV, Silverstein FS, Reindel FO, Penney JB, Young AB (1985) Muscarinic cholinergic receptors in human infant forebrain: [3H]quinuclidinyl benzilate binding in homogenates and quantitative autoradiography in sections. Dev Brain Res 19: 195–203
Kalaria RN, Fiedler C, Hunsaker JC, Sparks DL (1993) Synaptic neurochemistry of human striatum during development: changes in sudden infant death syndrome. J Neurochem 60: 2098–2105
Kim JS, Kornhuber HH, Schmid-Burgk W, Holzmüller B (1980) Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis of schizophrenia. Neurosci Lett 20: 379–382
Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy. II. Patterns of myalination in autopsied infants. J Neuropathol Exp Neurol 47: 217–234
Kinney HC, Filiano JJ, Harper RM (1992) The neuropathology of the sudden infant death syndrome. A review. J Neuropathol Exp Neurol 51: 115–126
Klekamp J, Riedel A, Harper C, Kretschmann HJ (1989) Morphometric study on the growth of non-cortical brain regions in Australian Aborigines and Caucasians. Brain Res 485: 79–88
Klekamp J, Riedel A, Harper C, Kretschmann HJ (1994) Morphometric study on the postnatal growth of the visual cortex of Australian Aborigines and Caucasians. J Brain Res 4: 541–548
Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260: 95–97
Konradi Ch, Komhuber J, Sofie E, Heckers S, Riederer P, Beckmann H (1992) Variations of monoamines and their metabolites in the human brain putamen. Brain Res 579: 285–290
Komhuber J, Konradi Ch, Mack-Burkhardt F, Riederer P, Heinsen H, Beckmann H (1989c) Ontogenesis of monoamine oxidase-A and -B in the human brain frontal cortex. Brain Res 499: 81–86
Kornhuber J, Mack-Burkhardt F, Konradi C, Fritze J, Riederer P (1989a) Effect of antemortem and postmortem factors on [3H]MK-801 binding in the human brain: transient elevation during early childhood. Life Sci 45: 745–749
Kornhuber J, Mack-Burkhardt F, Kornhuber ME, Riederer P (1989b) [3H]MK-801 binding sites in post-mortem human frontal cortex. Eur J Pharmacol 162: 483–490
Kornhuber J, Retz W, Riederer P, Heinsen H, Fritze J (1988) Effect of antemortem and postmortem factors on [3H] glutamate binding in the human brain. Neurosci Lett 93: 312–317
Kornhuber J, Riederer P (1991) Glutamate and schizophrenia. In: Racagni G (ed) Biological psychiatry, vol 1. Elsevier Science Publisher, Amsterdam, pp 495–497
Kornhuber ME, Kornhuber J, Retz W, Riederer P (1993) L-Glutamate and L-aspartate concentrations in the developing and aging human putamen tissue. J Neural Transm [Gen Sect] 93: 145–150
Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M (1992) Molecular diversity of the NMDA receptor channel. Nature 358: 36–41
Lanius RA, Pasqualotto BA, Shaw CA (1993) Age-dependent expression, phosphorylation and function of neurotransmitter receptors: pharmacological implications. Trends Pharmacol Sci 14: 403–408
Lauder JM (1988) Neurotransmitters as morphogens. Prog Brain Res 73: 365–387
Lavoie J, Giguère J-F, Layrargues GP, Butterworth RF (1987) Amino acid changes in autopsied brain tissue from cirrhotic patients with hepatic encephalopathy. J Neurochem 49: 692–697
Lee H, Choi BH (1992) Density and distribution of excitatory amino acid receptors in the developing human fetal brain: a quantitative autoradiographic study. Exp Neurol 118: 284–290
Lipton SA, Kater SB (1989) Neurotransmitter regulation neuronal outgrowth, plasticity and survival. Trends Neurosci 12: 265–270
Lovinger DM (1993) Excitotoxicity and alcohol-related brain damage. Alcohol Clin Exp Res 17: 19–27
Marcusson J, Oreland L, Winblad B (1984) Effect of age on human brain serotonin (S-1) binding sites. J Neurochem 43: 1699–1705
Mattson MP (1988) Neurotransmitter in the regulation of neuronal cytoarchitecture. Brain Res Rev 13: 179–212
Mattson MP, Hauser KF (1991) Spatial and temporal integration of neurotransmitter signals in the development of neural circuitry. Neurochem Int 19: 17–24
Mattson MP, Rychlik B, You JS, Sisken JE (1991) Sensitivity of cultured human embryonic cerebral cortical neurons to excitatory amino acid — induced calcium influx and neurotoxicity. Brain Res 542: 97–106
McDonald JW, Johnston MV (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 15: 41–70
Michaelis EK, Freed WJ, Galton N, Foye J, Michaelis ML, Phillips I, Kleinman JE (1990) Glutamate receptor changes in brain synaptic membranes from human alcoholics. Neurochem Res 15: 1055–1063
Michel AE, Garey LJ (1984) The development of dendritic spines in the human visual cortex. Hum Neurobiol 3: 223–227
Molliver ME, Kostovic I, van der Loos H (1973) The development of synapses in cerebral cortex of the human fetus. Brain Res 50: 403–407
Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Limeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256: 1217–1221
Murray RM, O'Callaghan E, Castle DJ, Lewis SW (1992) A neurodevelopmental ap proach to the classification of schizophrenia. Schizophr Bull 18: 319–332
Okumura N, Otsuki S, Kameyama A (1960) Studies on free amino acids in human brain. J Biochem 47: 315–320
O'Kusky JR, Norman MG (1992) Sudden infant death syndrome: postnatal changes in the numerical density and total number of neurons in the hypoglossal nucleus. J Neuropathol Exp Neurol 51: 577–584
Olney JW (1989) Excitatory amino acids and neuropsychiatrie disorders. Biol Psychiatry 26: 505–525
Olney JW (1991) Excitotoxicity and neuropsychiatric disorders. In: Ascher P, Choi DW, Christen Y (eds) Glutamate, cell death and memory. Springer, Berlin Heidelberg New York Tokyo, pp 77–101
Perry TL (1982) Cerebral amino acid pools. In: Lajtha A (ed) Handbook of neurochemistry, vol 1. Plenum Press, New York, pp 151–180
Perry TL, Hansen S, Gandham SS (1981) Postmortem changes of amino acid compounds in human and rat brain. J Neurochem 36: 406–412
Piggott MA, Perry EK, Perry RH, Court JA (1992) [3H]MK-801 binding to the NMDA receptor complex, and its modulation in human frontal cortex during development and aging. Brain Res 588: 277–286
Pollard H, Khrestchatisky M, Moreau J, Ben Ari Y (1993) Transient expression of the NR2C subunit of the NMDA receptor in developing rat brain. Neuro Report 4: 411–414
Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210: 153–157
Rabacchi S, Bailly Y, Delhaye-Bouchaud, Mariani J (1992) Involvment of the N-methyl-D-aspartate receptor in synapse elimination during cerebellar development. Science 256: 1823–1825
Ravi Kumar BV, Sastry PS (1985a) Muscarinic cholinergic receptors in human foetal brain: characterization and ontogeny of [3H]quinuclidinyl benzilate binding sites in frontal cortex. J Neurochem 44: 240–246
Ravi Kumar BV, Sastry PS (1985b) Muscarinic cholinergic receptors in human foetal brain: characterization and ontogeny of [3H]quinuclidinyl benzilate binding sites in corpus striatum, brainstem, and cerebellum. J Neurochem 45: 1948–1950
Ravi Kumar BV, Sastry PS (1992) Dopamine receptors in human foetal brains: characterization, regulation and ontogeny of [3H]spiperone binding sites in striatum. Neurochem Int 20: 559–566
Reichelt R, Hofmann D, Födisch H-J, Möhler H, Knapp M, Hebebrand J (1991) Ontogeny of the benzodiazepine receptor in human brain: fluorographic, immunochemical, and reversible binding studies. J Neurochem 57: 1128–1135
Represa A, Tremblay E, Ben-Ari Y (1989) Transient increase of NMDA-binding sites in human hippocampus during development. Neurosci Lett 99: 61–66
Represa A, Tremblay E, Schoevart D, Ben-Ari Y (1986) Development of high affinity kainate binding sites in human and rat hippocampi. Brain Res 384: 170–174
Riedel A, Klekamp J, Harper C, Kretschmann HJ (1989) Morphometric study on the postnatal growth of the cerebellar cortex of Australian Aborigines and Caucasians. Brain Res 499: 333–343
Riedel A, Klekamp J, Harper C, Kretschmann HJ (1994) Morphometric study on the postnatal growth of the cerebral cortex of Australian Aborigines and Caucasians. J Brain Res 35: 531–540
Rinne JO (1987) Muscarinic and dopaminergic receptors in the aging human brain. Brain Res 404: 162–168
Rinne JO, Lönnberg P, Marjamäki P (1990) Age-dependent decline in human brain dopamine Dl and D2 receptors. Brain Res 508: 349–352
Rothmann SM, Olney JW (1987) Excitotoxicity and the NMDA receptor. TINS 10: 299–302
Seeburg PH (1993) The molecular biology of mammalian glutamate receptor channels. TINS 16: 359–365
Seeman P, Bzowej NH, Guan H-C, Bergeron C, Becker LE, Reynolds GP, Bird ED, Riederer P, Jellinger K, Watanabe S, Tourtellotte WW (1987) Human brain dopamine receptors in children and aging adults. Synapse 1: 399–404
Shank RP, Campbell G (1983) Glutamate. In: Lajtha A (ed) Handbook of neurochemistry, vol 3. Plenum Press, New York, pp 381–422
Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368: 144–147
Sherriffs HJ, Olverman HJ, Thomson HE, Yates CM, Butterworth J, Butcher SP (1993) Developmental changes in [3H]MK801 binding to human frontal cortex. J Neurochem 61 [Suppl]: S196B
Slater P, McConnell S, D'Souza SW, Barson AJ (1992a) Age-related changes in binding to excitatory amino acid uptake sites in human cerebellum. Brain Res 579: 219–226
Slater P, McConnell S, D'Souza SW, Barson AJ (1993) Postnatal changes in N-methyl-D-aspartate receptor binding and stimulation by glutamate and glycine of [3H]MK-801 binding in human temporal cortex. Br J Pharmacol 108: 1143–1149
Slater P, McConnell S, D'Souza SW, Barson AJ, Simpson MDC, Gilchrist AC (1992b) Age-related changes in binding to excitatory amino acid uptake site in temporal cortex of human brain. Dev Brain Res 65: 157–160
Stanfield BB (1984) Postnatal reorganization of cortical projections: the role of collateral elimination. TINS 7: 37–41
Sturman JA, Gaull GE (1975) Taurine in the brain and liver of the developing human and monkey. J Neurochem 25: 831–835
Watson CG, Kucala T, Tilleskjor C, Jakobs L (1984) Schizophrenic birth seasonality in relation to the incidence of infectious diseases an temperature extremes. Arch Gen Psychiatry 41: 85–95
Willinger M, James LS, Catz C (1991) Defining the sudden infant death syndrome (SIDS): deliberations of an expert panel convened by the National Institute of Child Health and Human Development. Pediatr Pathol 11: 677–684
Wong EHF, Knight AR, Ransom R (1987) Glycine modulates [3H]MK-801 binding to the NMDA receptor in rat brain. Eur J Pharmacol 142: 487–488
Wroblewski JT, Danysz W (1989) Modulation of glutamate receptors: molecular mechanisms and functional implications. Annu Rev Pharmacol Toxicol 29: 441–474
Zukin RS, Pellegrini-Giampietro DE, McGurk JF, Bennett MVL (1992) Molecular biological studies of glutamate receptors in the developing brain. In: Simon RP (ed) Excitatory amino acids. Fidia Research Foundation Symposium Series, vol 9. Thieme Medical Publishers, New York, pp 47–51
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Retz, W., Kornhuber, J. & Riederer, P. Neurotransmission and the ontogeny of human brain. J. Neural Transmission 103, 403–419 (1996). https://doi.org/10.1007/BF01276417
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01276417