DOI: 10.1111/j.1471-4159.1988.tb02500.x. Selective Destruction of Cultured Dopaminergic Neurons from Fetal Rat Mesencephalon by 1‐Methyl‐4‐Phenylpyridinium: Cytochemical and Morphological Evidence

Selective Destruction of Cultured Dopaminergic Neurons from Fetal Rat Mesencephalon by 1‐Methyl‐4‐Phenylpyridinium: Cytochemical and Morphological Evidence

10.1111/j.1471-4159.1988.tb02500.x

Crossref journal-article

Wiley

Journal of Neurochemistry (311)

Abstract

Abstract: Dopaminergic neurons in cultures of dissociated cells from fetal rat mesencephalon were exposed to the principal metabolite of the neurotoxin 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP), 1‐methyl‐4‐phenyl‐pyridinium ion (MPP+), and several of its structural analogues. At concentrations between 0.01 and 0.1 μM, MPP+ inhibited catecholamine accumulation as visualized by cytofluorescence. Between 0.1 and 10.0 μM, MPP+ resulted in disappearance of tyrosine hydroxylase immunoreactivity without affecting other cells in the cultures. At concentrations higher than 10 μM, MPP+ was toxic to all cells present in the cultures. The effect of low concentrations of MPP+ on catecholamine cytofluorescence of the dopaminergic neurons was partially reversible. The intermediate concentrations produced irreversible structural changes of tyrosine hydroxylase‐positive cells, resulting in complete disappearance of these neurons. The morphological changes were specific to the dopaminergic neurons and were not evident in other cells viewed with phase contrast microscopy. Of the structural analogues tested, the 1‐ethyl analogue of MPP+ was effective in selectively destroying dopaminergic neurons in our culture system. The antioxidants l‐acetylcarnitine, β‐carotene, and α‐tocopherol failed to protect against MPP+ neurotoxicity when co‐incubated with the toxin.

Bibliography

SanchezâRamos, J. R., Michel, P., Weiner, W. J., & Hefti, F. (1988). Selective Destruction of Cultured Dopaminergic Neurons from Fetal Rat Mesencephalon by 1âMethylâ4âPhenylpyridinium: Cytochemical and Morphological Evidence. Journal of Neurochemistry, 50(6), 1934â1944. Portico.

Authors 4

Juan R. Sanchez‐Ramos (first)
Patrick Michel (additional)
William J. Weiner (additional)
Franz Hefti (additional)

References 64 Referenced 80

10.1016/0006-2952(84)90682-8
10.1016/0306-4522(82)90160-9
10.1073/pnas.80.14.4546
10.1016/0024-3205(85)90063-3
10.1016/0006-8993(86)91050-4
10.1016/0014-2999(84)90221-8
{'key': 'e_1_2_2_8_1', 'first-page': '77', 'article-title': 'Oxy‐radical toxicity in catecholamine neurons', 'volume': '5', 'author': 'Cohen G.', 'year': '1984', 'journal-title': 'Neurotoxicology'} / Neurotoxicology / Oxy‐radical toxicity in catecholamine neurons by Cohen G. (1984)
10.1016/0024-3205(85)90065-7
10.1016/0014-2999(84)90700-3
10.1038/327324a0
10.1016/0165-1781(79)90006-4
10.1016/0165-0270(80)90029-1
10.1016/0306-4522(76)90095-6
10.1016/0014-2999(84)90028-1
10.1002/ana.410200403
10.1016/0014-2999(84)90521-1
10.1111/j.1471-4159.1985.tb07120.x
{'key': 'e_1_2_2_19_1', 'first-page': '669', 'article-title': 'On the mechanisms underlying 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP) neurotoxicity: the effect of perinigral infusion of MPTP, its metabolite and their analogs in the rat', 'volume': '241', 'author': 'Harik S. I.', 'year': '1987', 'journal-title': 'J. Pharmacol. Exp. Ther.'} / J. Pharmacol. Exp. Ther. / On the mechanisms underlying 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP) neurotoxicity: the effect of perinigral infusion of MPTP, its metabolite and their analogs in the rat by Harik S. I. (1987)
{'key': 'e_1_2_2_20_1', 'first-page': '241', 'article-title': 'Further studies on the generation of hydrogen peroxide by 6‐OHdopamine: potentiation by ascorbic acid', 'volume': '8', 'author': 'Heikkila R. E.', 'year': '1972', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Further studies on the generation of hydrogen peroxide by 6‐OHdopamine: potentiation by ascorbic acid by Heikkila R. E. (1972)
10.1007/BF01946168
10.1126/science.6610213
10.1016/0028-3908(84)90170-9
10.1038/311467a0
10.1111/j.1471-4159.1985.tb05522.x
10.1016/0304-3940(85)90342-8
10.1016/0304-3940(85)90509-9
10.1016/0006-8993(86)90636-0
10.1016/0014-2999(84)90740-4
10.1016/0304-3940(84)90467-1
10.1016/0024-3205(85)90062-1
10.1073/pnas.84.10.3521
10.1126/science.6857258
10.1212/WNL.36.8.1147-b
10.1126/science.6823561
10.1126/science.6332378
10.1016/0304-3940(84)90501-9
10.1016/0006-8993(84)90777-7
{'key': 'e_1_2_2_39_1', 'first-page': '229', 'volume-title': 'Chemical Neuroanatomy', 'author': 'Lindvall O.', 'year': '1983'} / Chemical Neuroanatomy by Lindvall O. (1983)
10.1038/311464a0
10.1016/0304-3940(86)90602-6
10.1111/j.1471-4159.1986.tb00722.x
10.1016/0304-3940(87)90656-2
10.1126/science.6610939
10.1111/j.1471-4159.1985.tb10556.x
10.1016/0304-3940(85)90034-5
10.1016/0024-3205(85)90146-8
10.1016/0304-3940(85)90229-0
10.1016/0028-3908(85)90114-5
10.1016/0304-3940(85)90276-9
10.1016/0006-291X(86)90972-1
10.1016/0304-3940(87)90543-X
10.1016/0006-8993(86)90905-4
10.1016/0304-3940(84)90016-8
10.1016/0304-3940(86)90083-2
10.1016/0006-8993(88)91611-3
10.1016/0028-3908(85)90163-7
10.1111/j.1471-4159.1987.tb03384.x
10.1212/WNL.36.2.250
{'key': 'e_1_2_2_60_1', 'first-page': '631', 'article-title': 'Neurotoxic damage to nigrostriatal system following intranigral administration of the oxidative metabolites (MPDP and MPP) of MPTP', 'volume': '11', 'author': 'Sun C. J.', 'year': '1985', 'journal-title': 'Soc. Neurosci. Abstr.'} / Soc. Neurosci. Abstr. / Neurotoxic damage to nigrostriatal system following intranigral administration of the oxidative metabolites (MPDP and MPP) of MPTP by Sun C. J. (1985)
10.1111/j.1471-4159.1986.tb01768.x
10.1016/0028-3908(85)90164-9
10.1016/0028-3908(86)90184-X
10.1016/0024-3205(84)90112-7
10.1016/0304-3940(86)90012-1

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:33 p.m.)
Deposited	1 year, 10 months ago (Oct. 22, 2023, 1:27 a.m.)
Indexed	4 months, 3 weeks ago (April 8, 2025, 8:01 p.m.)
Issued	37 years, 3 months ago (June 1, 1988)
Published	37 years, 3 months ago (June 1, 1988)
Published Online	18 years, 10 months ago (Oct. 5, 2006)
Published Print	37 years, 3 months ago (June 1, 1988)

Funders 0

None

BibTeX

@article{Sanchez_Ramos_1988, title={Selective Destruction of Cultured Dopaminergic Neurons from Fetal Rat Mesencephalon by 1‐Methyl‐4‐Phenylpyridinium: Cytochemical and Morphological Evidence}, volume={50}, ISSN={1471-4159}, url={http://dx.doi.org/10.1111/j.1471-4159.1988.tb02500.x}, DOI={10.1111/j.1471-4159.1988.tb02500.x}, number={6}, journal={Journal of Neurochemistry}, publisher={Wiley}, author={Sanchez‐Ramos, Juan R. and Michel, Patrick and Weiner, William J. and Hefti, Franz}, year={1988}, month=jun, pages={1934–1944} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        4,
        9
      ]
    ],
    "date-time": "2025-04-09T00:01:25Z",
    "timestamp": 1744156885361
  },
  "reference-count": 64,
  "publisher": "Wiley",
  "issue": "6",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2006,
            10,
            5
          ]
        ],
        "date-time": "2006-10-05T00:00:00Z",
        "timestamp": 1160006400000
      },
      "content-version": "vor",
      "delay-in-days": 6700,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1988,
        6
      ]
    ]
  },
  "abstract": "<jats:p><jats:bold>Abstract: </jats:bold> Dopaminergic neurons in cultures of dissociated cells from fetal rat mesencephalon were exposed to the principal metabolite of the neurotoxin 1\u2010methyl\u20104\u2010phenyl\u20101,2,3,6\u2010tetrahydropyridine (MPTP), 1\u2010methyl\u20104\u2010phenyl\u2010pyridinium ion (MPP<jats:sup>+</jats:sup>), and several of its structural analogues. At concentrations between 0.01 and 0.1 \u03bc<jats:italic>M</jats:italic>, MPP<jats:sup>+</jats:sup> inhibited catecholamine accumulation as visualized by cytofluorescence. Between 0.1 and 10.0 \u03bc<jats:italic>M</jats:italic>, MPP<jats:sup>+</jats:sup> resulted in disappearance of tyrosine hydroxylase immunoreactivity without affecting other cells in the cultures. At concentrations higher than 10 \u03bc<jats:italic>M</jats:italic>, MPP<jats:sup>+</jats:sup> was toxic to all cells present in the cultures. The effect of low concentrations of MPP<jats:sup>+</jats:sup> on catecholamine cytofluorescence of the dopaminergic neurons was partially reversible. The intermediate concentrations produced irreversible structural changes of tyrosine hydroxylase\u2010positive cells, resulting in complete disappearance of these neurons. The morphological changes were specific to the dopaminergic neurons and were not evident in other cells viewed with phase contrast microscopy. Of the structural analogues tested, the 1\u2010ethyl analogue of MPP<jats:sup>+</jats:sup> was effective in selectively destroying dopaminergic neurons in our culture system. The antioxidants l\u2010acetylcarnitine, \u03b2\u2010carotene, and \u03b1\u2010tocopherol failed to protect against MPP<jats:sup>+</jats:sup> neurotoxicity when co\u2010incubated with the toxin.</jats:p>",
  "DOI": "10.1111/j.1471-4159.1988.tb02500.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T21:33:48Z",
    "timestamp": 1160084028000
  },
  "page": "1934-1944",
  "source": "Crossref",
  "is-referenced-by-count": 80,
  "title": "Selective Destruction of Cultured Dopaminergic Neurons from Fetal Rat Mesencephalon by 1\u2010Methyl\u20104\u2010Phenylpyridinium: Cytochemical and Morphological Evidence",
  "prefix": "10.1111",
  "volume": "50",
  "author": [
    {
      "given": "Juan R.",
      "family": "Sanchez\u2010Ramos",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Patrick",
      "family": "Michel",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "William J.",
      "family": "Weiner",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Franz",
      "family": "Hefti",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_2_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-2952(84)90682-8"
    },
    {
      "key": "e_1_2_2_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(82)90160-9"
    },
    {
      "key": "e_1_2_2_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.14.4546"
    },
    {
      "key": "e_1_2_2_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(85)90063-3"
    },
    {
      "key": "e_1_2_2_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(86)91050-4"
    },
    {
      "key": "e_1_2_2_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(84)90221-8"
    },
    {
      "key": "e_1_2_2_8_1",
      "first-page": "77",
      "article-title": "Oxy\u2010radical toxicity in catecholamine neurons",
      "volume": "5",
      "author": "Cohen G.",
      "year": "1984",
      "journal-title": "Neurotoxicology"
    },
    {
      "key": "e_1_2_2_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(85)90065-7"
    },
    {
      "key": "e_1_2_2_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(84)90700-3"
    },
    {
      "key": "e_1_2_2_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/327324a0"
    },
    {
      "key": "e_1_2_2_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-1781(79)90006-4"
    },
    {
      "key": "e_1_2_2_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0165-0270(80)90029-1"
    },
    {
      "key": "e_1_2_2_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0306-4522(76)90095-6"
    },
    {
      "key": "e_1_2_2_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(84)90028-1"
    },
    {
      "key": "e_1_2_2_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ana.410200403"
    },
    {
      "key": "e_1_2_2_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(84)90521-1"
    },
    {
      "key": "e_1_2_2_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1985.tb07120.x"
    },
    {
      "key": "e_1_2_2_19_1",
      "first-page": "669",
      "article-title": "On the mechanisms underlying 1\u2010methyl\u20104\u2010phenyl\u20101,2,3,6\u2010tetrahydropyridine (MPTP) neurotoxicity: the effect of perinigral infusion of MPTP, its metabolite and their analogs in the rat",
      "volume": "241",
      "author": "Harik S. I.",
      "year": "1987",
      "journal-title": "J. Pharmacol. Exp. Ther."
    },
    {
      "key": "e_1_2_2_20_1",
      "first-page": "241",
      "article-title": "Further studies on the generation of hydrogen peroxide by 6\u2010OHdopamine: potentiation by ascorbic acid",
      "volume": "8",
      "author": "Heikkila R. E.",
      "year": "1972",
      "journal-title": "Mol. Pharmacol."
    },
    {
      "key": "e_1_2_2_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01946168"
    },
    {
      "key": "e_1_2_2_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6610213"
    },
    {
      "key": "e_1_2_2_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(84)90170-9"
    },
    {
      "key": "e_1_2_2_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/311467a0"
    },
    {
      "key": "e_1_2_2_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1985.tb05522.x"
    },
    {
      "key": "e_1_2_2_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(85)90342-8"
    },
    {
      "key": "e_1_2_2_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(85)90509-9"
    },
    {
      "key": "e_1_2_2_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(86)90636-0"
    },
    {
      "key": "e_1_2_2_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-2999(84)90740-4"
    },
    {
      "key": "e_1_2_2_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(84)90467-1"
    },
    {
      "key": "e_1_2_2_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(85)90062-1"
    },
    {
      "key": "e_1_2_2_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.84.10.3521"
    },
    {
      "key": "e_1_2_2_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6857258"
    },
    {
      "key": "e_1_2_2_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1212/WNL.36.8.1147-b"
    },
    {
      "key": "e_1_2_2_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6823561"
    },
    {
      "key": "e_1_2_2_36_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6332378"
    },
    {
      "key": "e_1_2_2_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(84)90501-9"
    },
    {
      "key": "e_1_2_2_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(84)90777-7"
    },
    {
      "key": "e_1_2_2_39_1",
      "first-page": "229",
      "volume-title": "Chemical Neuroanatomy",
      "author": "Lindvall O.",
      "year": "1983"
    },
    {
      "key": "e_1_2_2_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/311464a0"
    },
    {
      "key": "e_1_2_2_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(86)90602-6"
    },
    {
      "key": "e_1_2_2_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1986.tb00722.x"
    },
    {
      "key": "e_1_2_2_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(87)90656-2"
    },
    {
      "key": "e_1_2_2_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6610939"
    },
    {
      "key": "e_1_2_2_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1985.tb10556.x"
    },
    {
      "key": "e_1_2_2_46_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(85)90034-5"
    },
    {
      "key": "e_1_2_2_47_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(85)90146-8"
    },
    {
      "key": "e_1_2_2_48_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(85)90229-0"
    },
    {
      "key": "e_1_2_2_49_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(85)90114-5"
    },
    {
      "key": "e_1_2_2_50_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(85)90276-9"
    },
    {
      "key": "e_1_2_2_51_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(86)90972-1"
    },
    {
      "key": "e_1_2_2_52_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(87)90543-X"
    },
    {
      "key": "e_1_2_2_53_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(86)90905-4"
    },
    {
      "key": "e_1_2_2_54_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(84)90016-8"
    },
    {
      "key": "e_1_2_2_55_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(86)90083-2"
    },
    {
      "key": "e_1_2_2_56_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(88)91611-3"
    },
    {
      "key": "e_1_2_2_57_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(85)90163-7"
    },
    {
      "key": "e_1_2_2_58_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1987.tb03384.x"
    },
    {
      "key": "e_1_2_2_59_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1212/WNL.36.2.250"
    },
    {
      "key": "e_1_2_2_60_1",
      "first-page": "631",
      "article-title": "Neurotoxic damage to nigrostriatal system following intranigral administration of the oxidative metabolites (MPDP and MPP) of MPTP",
      "volume": "11",
      "author": "Sun C. J.",
      "year": "1985",
      "journal-title": "Soc. Neurosci. Abstr."
    },
    {
      "key": "e_1_2_2_61_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1986.tb01768.x"
    },
    {
      "key": "e_1_2_2_62_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(85)90164-9"
    },
    {
      "key": "e_1_2_2_63_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3908(86)90184-X"
    },
    {
      "key": "e_1_2_2_64_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0024-3205(84)90112-7"
    },
    {
      "key": "e_1_2_2_65_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(86)90012-1"
    }
  ],
  "container-title": "Journal of Neurochemistry",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1471-4159.1988.tb02500.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1471-4159.1988.tb02500.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        22
      ]
    ],
    "date-time": "2023-10-22T05:27:56Z",
    "timestamp": 1697952476000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1111/j.1471-4159.1988.tb02500.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1988,
        6
      ]
    ]
  },
  "references-count": 64,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          1988,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1471-4159.1988.tb02500.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1471-4159.1988.tb02500.x",
  "relation": {},
  "ISSN": [
    "0022-3042",
    "1471-4159"
  ],
  "subject": [],
  "container-title-short": "Journal of Neurochemistry",
  "published": {
    "date-parts": [
      [
        1988,
        6
      ]
    ]
  }
}