DOI: 10.1126/science.1688664. Survival of Adult Basal Forebrain Cholinergic Neurons After Loss of Target Neurons

Survival of Adult Basal Forebrain Cholinergic Neurons After Loss of Target Neurons

10.1126/science.1688664

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Target cells are thought to regulate the survival of afferent neurons during development by supplying limiting amounts of neurotrophic factors, but the degree to which afferent neurons remain dependent on target-derived support in the adult is uncertain. In this study, uninjured basal forebrain cholinergic neurons did not die after excitotoxic ablation of their target neurons in young adult rats, indicating that they are either not dependent on neurotrophic factors for survival or can obtain trophic support from other sources after target neurons are lost. This finding suggests that cholinergic cell death in neurodegenerative conditions such as Alzheimer's disease is not due solely to a loss of target neurons or factors provided by them.

Bibliography

Sofroniew, M. V., Galletly, N. P., Isacson, O., & Svendsen, C. N. (1990). Survival of Adult Basal Forebrain Cholinergic Neurons After Loss of Target Neurons. Science, 247(4940), 338â342.

Authors 4

Michael V. Sofroniew (first)
Neil P. Galletly (additional)
Ole Isacson (additional)
Clive N. Svendsen (additional)

References 43 Referenced 237

ABERCROMBIE, M, ESTIMATION OF NUCLEAR POPULATION FROM MICROTOME SECTIONS, ANATOMICAL RECORD 94: 239 (1946). (10.1002/ar.1090940210) / ANATOMICAL RECORD (1946)
AMARAL, D.G., AN ANALYSIS OF THE ORIGINS OF THE CHOLINERGIC AND NONCHOLINERGIC SEPTAL PROJECTIONS TO THE HIPPOCAMPAL-FORMATION OF THE RAT, JOURNAL OF COMPARATIVE NEUROLOGY 240: 37 (1985). (10.1002/cne.902400104) / JOURNAL OF COMPARATIVE NEUROLOGY (1985)
ANDERSON, K.J., BASIC FIBROBLAST GROWTH-FACTOR PREVENTS DEATH OF LESIONED CHOLINERGIC NEURONS INVIVO, NATURE 332: 360 (1988). (10.1038/332360a0) / NATURE (1988)
APPEL, S.H., A UNIFYING HYPOTHESIS FOR THE CAUSE OF AMYOTROPHIC LATERAL SCLEROSIS, PARKINSONISM, AND ALZHEIMER-DISEASE, ANNALS OF NEUROLOGY 10: 499 (1981). (10.1002/ana.410100602) / ANNALS OF NEUROLOGY (1981)
ARENDT, T, NEURONAL LOSS IN DIFFERENT PARTS OF THE NUCLEUS BASALIS IS RELATED TO NEURITIC PLAQUE-FORMATION IN CORTICAL TARGET AREAS IN ALZHEIMERS-DISEASE, NEUROSCIENCE 14: 1 (1985). (10.1016/0306-4522(85)90160-5) / NEUROSCIENCE (1985)
10.1126/science.2897715
BARDE, Y.A., TROPHIC FACTORS AND NEURONAL SURVIVAL, NEURON 2: 1525 (1989). (10.1016/0896-6273(89)90040-8) / NEURON (1989)
BJERRE, B, SHORT-TERM AND LONG-TERM EFFECTS OF NERVE GROWTH-FACTOR ON SYMPATHETIC NERVOUS-SYSTEM IN ADULT MOUSE, BRAIN RESEARCH 94: 263 (1975). (10.1016/0006-8993(75)90061-X) / BRAIN RESEARCH (1975)
10.1126/science.7292000
CHANDLER, C.E., A MONOCLONAL-ANTIBODY MODULATES THE INTERACTION OF NERVE GROWTH-FACTOR WITH PC12 CELLS, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 6882 (1984). (10.1016/S0021-9258(17)39810-1) / JOURNAL OF BIOLOGICAL CHEMISTRY (1984)
10.1126/science.6474175
10.1038/329065a0
GAGE, F.H., RETROGRADE CELL CHANGES IN MEDIAL SEPTUM AND DIAGONAL BAND FOLLOWING FIMBRIA-FORNIX TRANSECTION - QUANTITATIVE TEMPORAL ANALYSIS, NEUROSCIENCE 19: 241 (1986). (10.1016/0306-4522(86)90018-7) / NEUROSCIENCE (1986)
GAHWILER, B.H., NERVE GROWTH-FACTOR PROMOTES DEVELOPMENT OF THE RAT SEPTOHIPPOCAMPAL CHOLINERGIC PROJECTION INVITRO, NEUROSCIENCE LETTERS 75: 6 (1987). (10.1016/0304-3940(87)90066-8) / NEUROSCIENCE LETTERS (1987)
GOEDERT, M, NERVE GROWTH-FACTOR MESSENGER-RNA IN PERIPHERAL AND CENTRAL RAT-TISSUES AND IN THE HUMAN CENTRAL-NERVOUS-SYSTEM - LESION EFFECTS IN THE RAT-BRAIN AND LEVELS IN ALZHEIMERS-DISEASE, MOLECULAR BRAIN RESEARCH 1: 85 (1986). (10.1016/0169-328X(86)90023-9) / MOLECULAR BRAIN RESEARCH (1986)
GOLDSCHMIDT, R.B., TIME COURSE OF INCREASES IN RETROGRADE LABELING AND INCREASES IN CELL-SIZE OF ENTORHINAL CORTEX NEURONS SPROUTING IN RESPONSE TO UNILATERAL ENTORHINAL LESIONS, JOURNAL OF COMPARATIVE NEUROLOGY 189: 359 (1980). (10.1002/cne.901890210) / JOURNAL OF COMPARATIVE NEUROLOGY (1980)
HARTIKKA, J, DEVELOPMENT OF SEPTAL CHOLINERGIC NEURONS IN CULTURE - PLATING DENSITY AND GLIAL-CELLS MODULATE EFFECTS OF NGF ON SURVIVAL, FIBER GROWTH, AND EXPRESSION OF TRANSMITTER-SPECIFIC ENZYMES, JOURNAL OF NEUROSCIENCE 8: 2967 (1988). (10.1523/JNEUROSCI.08-08-02967.1988) / JOURNAL OF NEUROSCIENCE (1988)
HEFTI, F, IS ALZHEIMER-DISEASE CAUSED BY LACK OF NERVE GROWTH-FACTOR, ANNALS OF NEUROLOGY 13: 109 (1983). (10.1002/ana.410130127) / ANNALS OF NEUROLOGY (1983)
HEFTI, F, NERVE GROWTH-FACTOR PROMOTES SURVIVAL OF SEPTAL CHOLINERGIC NEURONS AFTER FIMBRIAL TRANSECTIONS, JOURNAL OF NEUROSCIENCE 6: 2155 (1986). (10.1523/JNEUROSCI.06-08-02155.1986) / JOURNAL OF NEUROSCIENCE (1986)
HEFTI, F, NERVE GROWTH-FACTOR INCREASES CHOLINE ACETYL-TRANSFERASE BUT NOT SURVIVAL OR FIBER OUTGROWTH OF CULTURED FETAL SEPTAL CHOLINERGIC NEURONS, NEUROSCIENCE 14: 55 (1985). (10.1016/0306-4522(85)90163-0) / NEUROSCIENCE (1985)
JOHNSON, E.M., THE ROLE OF NGF IN SENSORY NEURONS INVIVO, TRENDS IN NEUROSCIENCES 9: 33 (1986). (10.1016/0166-2236(86)90012-3) / TRENDS IN NEUROSCIENCES (1986)
KALEN, P, PROJECTIONS FROM THE MEDIAL SEPTUM AND DIAGONAL BAND OF BROCA TO THE DORSAL AND CENTRAL SUPERIOR RAPHE NUCLEI - A NON-CHOLINERGIC PATHWAY, EXPERIMENTAL BRAIN RESEARCH 75: 401 (1989). / EXPERIMENTAL BRAIN RESEARCH (1989)
KORSCHING, S, THE ROLE OF NERVE GROWTH-FACTOR IN THE CNS, TRENDS IN NEUROSCIENCES 9: 570 (1986). (10.1016/0166-2236(86)90179-7) / TRENDS IN NEUROSCIENCES (1986)
10.1126/science.3798108
LAMS, B.E., LOSS OF TRANSMITTER-ASSOCIATED ENZYME STAINING FOLLOWING AXOTOMY DOES NOT INDICATE DEATH OF BRAIN-STEM CHOLINERGIC NEURONS, BRAIN RESEARCH 475: 401 (1988). (10.1016/0006-8993(88)90635-X) / BRAIN RESEARCH (1988)
LIEBERMAN, A.R., INTERNATIONAL REVIEW OF NEUROBIOLOGY 14: 49 (1971). (10.1016/S0074-7742(08)60183-X) / INTERNATIONAL REVIEW OF NEUROBIOLOGY (1971)
LINDSAY, R.M., ADULT-RAT BRAIN ASTROCYTES SUPPORT SURVIVAL OF BOTH NGF-DEPENDENT AND NGF-INSENSITIVE NEURONS, NATURE 282: 80 (1979). (10.1038/282080a0) / NATURE (1979)
Nieto-Sampedro, M., Proceedings of the National Academy of Sciences of the United States of America 81: 6250 (1984). / Proceedings of the National Academy of Sciences of the United States of America (1984)
OTTO, D, BASIC FIBROBLAST GROWTH-FACTOR AND NERVE GROWTH-FACTOR ADMINISTERED IN GEL FOAM RESCUE MEDIAL SEPTAL NEURONS AFTER FIMBRIA FORNIX TRANSECTION, JOURNAL OF NEUROSCIENCE RESEARCH 22: 83 (1989). (10.1002/jnr.490220111) / JOURNAL OF NEUROSCIENCE RESEARCH (1989)
PAXINOS G RAT BRAIN STEREOTAXI (1986).
PEARSON, RCA, PERSISTENCE OF CHOLINERGIC NEURONS IN THE BASAL NUCLEUS IN A BRAIN WITH SENILE DEMENTIA OF THE ALZHEIMERS TYPE DEMONSTRATED BY IMMUNOHISTOCHEMICAL STAINING FOR CHOLINE-ACETYLTRANSFERASE, BRAIN RESEARCH 289: 375 (1983). (10.1016/0006-8993(83)90046-X) / BRAIN RESEARCH (1983)
PURVES, D, TROPHIC REGULATION OF NERVE-CELL MORPHOLOGY AND INNERVATION IN THE AUTONOMIC NERVOUS-SYSTEM, NATURE 336: 123 (1988). (10.1038/336123a0) / NATURE (1988)
10.1126/science.3201248
10.1126/science.887924
SOFRONIEW, M.V., THE CHOLINERGIC NUCLEI OF THE BASAL FOREBRAIN OF THE RAT - NORMAL STRUCTURE, DEVELOPMENT AND EXPERIMENTALLY INDUCED DEGENERATION, BRAIN RESEARCH 411: 310 (1987). (10.1016/0006-8993(87)91084-5) / BRAIN RESEARCH (1987)
Sofroniew, M. V., Brain Research 476: 358 (1989). (10.1016/0006-8993(89)91259-6) / Brain Research (1989)
SOFRONIEW, M.V., J CHEM NEUROANAT 1: 327 (1988). / J CHEM NEUROANAT (1988)
SWANSON L.W. HDB CHEM NEUROANAT 1 5 (1987). (10.1097/00152193-198701000-00003)
VILLEGASPEREZ, M.P., INFLUENCES OF PERIPHERAL-NERVE GRAFTS ON THE SURVIVAL AND REGROWTH OF AXOTOMIZED RETINAL GANGLION-CELLS IN ADULT-RATS, JOURNAL OF NEUROSCIENCE 8: 265 (1988). (10.1523/JNEUROSCI.08-01-00265.1988) / JOURNAL OF NEUROSCIENCE (1988)
VILLEGASPEREZ, M.P., SOCIETY FOR NEUROSCIENCE. ABSTRACTS 14: 673 (1988). / SOCIETY FOR NEUROSCIENCE. ABSTRACTS (1988)
10.1126/science.7058341
WHITTEMORE, S.R., RAT BETA-NERVE GROWTH-FACTOR SEQUENCE AND SITE OF SYNTHESIS IN THE ADULT HIPPOCAMPUS, JOURNAL OF NEUROSCIENCE RESEARCH 20: 403 (1988). (10.1002/jnr.490200402) / JOURNAL OF NEUROSCIENCE RESEARCH (1988)
WILLIAMS, L.R., CONTINUOUS INFUSION OF NERVE GROWTH-FACTOR PREVENTS BASAL FOREBRAIN NEURONAL DEATH AFTER FIMBRIA FORNIX TRANSECTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 9231 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 6:10 p.m.)
Deposited	1 year, 7 months ago (Jan. 11, 2024, 10:23 a.m.)
Indexed	1 month, 1 week ago (July 20, 2025, 12:28 a.m.)
Issued	35 years, 7 months ago (Jan. 19, 1990)
Published	35 years, 7 months ago (Jan. 19, 1990)
Published Print	35 years, 7 months ago (Jan. 19, 1990)

Funders 0

None

BibTeX

@article{Sofroniew_1990, title={Survival of Adult Basal Forebrain Cholinergic Neurons After Loss of Target Neurons}, volume={247}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1688664}, DOI={10.1126/science.1688664}, number={4940}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Sofroniew, Michael V. and Galletly, Neil P. and Isacson, Ole and Svendsen, Clive N.}, year={1990}, month=jan, pages={338–342} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        20
      ]
    ],
    "date-time": "2025-07-20T04:28:32Z",
    "timestamp": 1752985712017
  },
  "reference-count": 43,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "4940",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1990,
        1,
        19
      ]
    ]
  },
  "abstract": "<jats:p>Target cells are thought to regulate the survival of afferent neurons during development by supplying limiting amounts of neurotrophic factors, but the degree to which afferent neurons remain dependent on target-derived support in the adult is uncertain. In this study, uninjured basal forebrain cholinergic neurons did not die after excitotoxic ablation of their target neurons in young adult rats, indicating that they are either not dependent on neurotrophic factors for survival or can obtain trophic support from other sources after target neurons are lost. This finding suggests that cholinergic cell death in neurodegenerative conditions such as Alzheimer's disease is not due solely to a loss of target neurons or factors provided by them.</jats:p>",
  "DOI": "10.1126/science.1688664",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T22:10:14Z",
    "timestamp": 1160086214000
  },
  "page": "338-342",
  "source": "Crossref",
  "is-referenced-by-count": 237,
  "title": "Survival of Adult Basal Forebrain Cholinergic Neurons After Loss of Target Neurons",
  "prefix": "10.1126",
  "volume": "247",
  "author": [
    {
      "given": "Michael V.",
      "family": "Sofroniew",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Anatomy, University of Cambridge, Cambridge, CB2 3DY, England."
        }
      ]
    },
    {
      "given": "Neil P.",
      "family": "Galletly",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy, University of Cambridge, Cambridge, CB2 3DY, England."
        }
      ]
    },
    {
      "given": "Ole",
      "family": "Isacson",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy, University of Cambridge, Cambridge, CB2 3DY, England."
        }
      ]
    },
    {
      "given": "Clive N.",
      "family": "Svendsen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Anatomy, University of Cambridge, Cambridge, CB2 3DY, England."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "239",
      "DOI": "10.1002/ar.1090940210",
      "volume": "94",
      "year": "1946",
      "unstructured": "ABERCROMBIE, M, ESTIMATION OF NUCLEAR POPULATION FROM MICROTOME SECTIONS, ANATOMICAL RECORD 94: 239 (1946).",
      "journal-title": "ANATOMICAL RECORD"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1002/cne.902400104",
      "volume": "240",
      "year": "1985",
      "unstructured": "AMARAL, D.G., AN ANALYSIS OF THE ORIGINS OF THE CHOLINERGIC AND NONCHOLINERGIC SEPTAL PROJECTIONS TO THE HIPPOCAMPAL-FORMATION OF THE RAT, JOURNAL OF COMPARATIVE NEUROLOGY 240: 37 (1985).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "crossref",
      "first-page": "360",
      "DOI": "10.1038/332360a0",
      "volume": "332",
      "year": "1988",
      "unstructured": "ANDERSON, K.J., BASIC FIBROBLAST GROWTH-FACTOR PREVENTS DEATH OF LESIONED CHOLINERGIC NEURONS INVIVO, NATURE 332: 360 (1988).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "499",
      "DOI": "10.1002/ana.410100602",
      "volume": "10",
      "year": "1981",
      "unstructured": "APPEL, S.H., A UNIFYING HYPOTHESIS FOR THE CAUSE OF AMYOTROPHIC LATERAL SCLEROSIS, PARKINSONISM, AND ALZHEIMER-DISEASE, ANNALS OF NEUROLOGY 10: 499 (1981).",
      "journal-title": "ANNALS OF NEUROLOGY"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0306-4522(85)90160-5",
      "volume": "14",
      "year": "1985",
      "unstructured": "ARENDT, T, NEURONAL LOSS IN DIFFERENT PARTS OF THE NUCLEUS BASALIS IS RELATED TO NEURITIC PLAQUE-FORMATION IN CORTICAL TARGET AREAS IN ALZHEIMERS-DISEASE, NEUROSCIENCE 14: 1 (1985).",
      "journal-title": "NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2897715"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "1525",
      "DOI": "10.1016/0896-6273(89)90040-8",
      "volume": "2",
      "year": "1989",
      "unstructured": "BARDE, Y.A., TROPHIC FACTORS AND NEURONAL SURVIVAL, NEURON 2: 1525 (1989).",
      "journal-title": "NEURON"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1016/0006-8993(75)90061-X",
      "volume": "94",
      "year": "1975",
      "unstructured": "BJERRE, B, SHORT-TERM AND LONG-TERM EFFECTS OF NERVE GROWTH-FACTOR ON SYMPATHETIC NERVOUS-SYSTEM IN ADULT MOUSE, BRAIN RESEARCH 94: 263 (1975).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7292000"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "6882",
      "DOI": "10.1016/S0021-9258(17)39810-1",
      "volume": "259",
      "year": "1984",
      "unstructured": "CHANDLER, C.E., A MONOCLONAL-ANTIBODY MODULATES THE INTERACTION OF NERVE GROWTH-FACTOR WITH PC12 CELLS, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 6882 (1984).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.6474175"
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/329065a0"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "241",
      "DOI": "10.1016/0306-4522(86)90018-7",
      "volume": "19",
      "year": "1986",
      "unstructured": "GAGE, F.H., RETROGRADE CELL CHANGES IN MEDIAL SEPTUM AND DIAGONAL BAND FOLLOWING FIMBRIA-FORNIX TRANSECTION - QUANTITATIVE TEMPORAL ANALYSIS, NEUROSCIENCE 19: 241 (1986).",
      "journal-title": "NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "6",
      "DOI": "10.1016/0304-3940(87)90066-8",
      "volume": "75",
      "year": "1987",
      "unstructured": "GAHWILER, B.H., NERVE GROWTH-FACTOR PROMOTES DEVELOPMENT OF THE RAT SEPTOHIPPOCAMPAL CHOLINERGIC PROJECTION INVITRO, NEUROSCIENCE LETTERS 75: 6 (1987).",
      "journal-title": "NEUROSCIENCE LETTERS"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "85",
      "DOI": "10.1016/0169-328X(86)90023-9",
      "volume": "1",
      "year": "1986",
      "unstructured": "GOEDERT, M, NERVE GROWTH-FACTOR MESSENGER-RNA IN PERIPHERAL AND CENTRAL RAT-TISSUES AND IN THE HUMAN CENTRAL-NERVOUS-SYSTEM - LESION EFFECTS IN THE RAT-BRAIN AND LEVELS IN ALZHEIMERS-DISEASE, MOLECULAR BRAIN RESEARCH 1: 85 (1986).",
      "journal-title": "MOLECULAR BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1002/cne.901890210",
      "volume": "189",
      "year": "1980",
      "unstructured": "GOLDSCHMIDT, R.B., TIME COURSE OF INCREASES IN RETROGRADE LABELING AND INCREASES IN CELL-SIZE OF ENTORHINAL CORTEX NEURONS SPROUTING IN RESPONSE TO UNILATERAL ENTORHINAL LESIONS, JOURNAL OF COMPARATIVE NEUROLOGY 189: 359 (1980).",
      "journal-title": "JOURNAL OF COMPARATIVE NEUROLOGY"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "2967",
      "DOI": "10.1523/JNEUROSCI.08-08-02967.1988",
      "volume": "8",
      "year": "1988",
      "unstructured": "HARTIKKA, J, DEVELOPMENT OF SEPTAL CHOLINERGIC NEURONS IN CULTURE - PLATING DENSITY AND GLIAL-CELLS MODULATE EFFECTS OF NGF ON SURVIVAL, FIBER GROWTH, AND EXPRESSION OF TRANSMITTER-SPECIFIC ENZYMES, JOURNAL OF NEUROSCIENCE 8: 2967 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "109",
      "DOI": "10.1002/ana.410130127",
      "volume": "13",
      "year": "1983",
      "unstructured": "HEFTI, F, IS ALZHEIMER-DISEASE CAUSED BY LACK OF NERVE GROWTH-FACTOR, ANNALS OF NEUROLOGY 13: 109 (1983).",
      "journal-title": "ANNALS OF NEUROLOGY"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "2155",
      "DOI": "10.1523/JNEUROSCI.06-08-02155.1986",
      "volume": "6",
      "year": "1986",
      "unstructured": "HEFTI, F, NERVE GROWTH-FACTOR PROMOTES SURVIVAL OF SEPTAL CHOLINERGIC NEURONS AFTER FIMBRIAL TRANSECTIONS, JOURNAL OF NEUROSCIENCE 6: 2155 (1986).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "55",
      "DOI": "10.1016/0306-4522(85)90163-0",
      "volume": "14",
      "year": "1985",
      "unstructured": "HEFTI, F, NERVE GROWTH-FACTOR INCREASES CHOLINE ACETYL-TRANSFERASE BUT NOT SURVIVAL OR FIBER OUTGROWTH OF CULTURED FETAL SEPTAL CHOLINERGIC NEURONS, NEUROSCIENCE 14: 55 (1985).",
      "journal-title": "NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "33",
      "DOI": "10.1016/0166-2236(86)90012-3",
      "volume": "9",
      "year": "1986",
      "unstructured": "JOHNSON, E.M., THE ROLE OF NGF IN SENSORY NEURONS INVIVO, TRENDS IN NEUROSCIENCES 9: 33 (1986).",
      "journal-title": "TRENDS IN NEUROSCIENCES"
    },
    {
      "key": "e_1_2_1_22_1",
      "first-page": "401",
      "volume": "75",
      "year": "1989",
      "unstructured": "KALEN, P, PROJECTIONS FROM THE MEDIAL SEPTUM AND DIAGONAL BAND OF BROCA TO THE DORSAL AND CENTRAL SUPERIOR RAPHE NUCLEI - A NON-CHOLINERGIC PATHWAY, EXPERIMENTAL BRAIN RESEARCH 75: 401 (1989).",
      "journal-title": "EXPERIMENTAL BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "570",
      "DOI": "10.1016/0166-2236(86)90179-7",
      "volume": "9",
      "year": "1986",
      "unstructured": "KORSCHING, S, THE ROLE OF NERVE GROWTH-FACTOR IN THE CNS, TRENDS IN NEUROSCIENCES 9: 570 (1986).",
      "journal-title": "TRENDS IN NEUROSCIENCES"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3798108"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1016/0006-8993(88)90635-X",
      "volume": "475",
      "year": "1988",
      "unstructured": "LAMS, B.E., LOSS OF TRANSMITTER-ASSOCIATED ENZYME STAINING FOLLOWING AXOTOMY DOES NOT INDICATE DEATH OF BRAIN-STEM CHOLINERGIC NEURONS, BRAIN RESEARCH 475: 401 (1988).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1016/S0074-7742(08)60183-X",
      "volume": "14",
      "year": "1971",
      "unstructured": "LIEBERMAN, A.R., INTERNATIONAL REVIEW OF NEUROBIOLOGY 14: 49 (1971).",
      "journal-title": "INTERNATIONAL REVIEW OF NEUROBIOLOGY"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "80",
      "DOI": "10.1038/282080a0",
      "volume": "282",
      "year": "1979",
      "unstructured": "LINDSAY, R.M., ADULT-RAT BRAIN ASTROCYTES SUPPORT SURVIVAL OF BOTH NGF-DEPENDENT AND NGF-INSENSITIVE NEURONS, NATURE 282: 80 (1979).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_28_1",
      "first-page": "6250",
      "volume": "81",
      "year": "1984",
      "unstructured": "Nieto-Sampedro, M., Proceedings of the National Academy of Sciences of the United States of America 81: 6250 (1984).",
      "journal-title": "Proceedings of the National Academy of Sciences of the United States of America"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "83",
      "DOI": "10.1002/jnr.490220111",
      "volume": "22",
      "year": "1989",
      "unstructured": "OTTO, D, BASIC FIBROBLAST GROWTH-FACTOR AND NERVE GROWTH-FACTOR ADMINISTERED IN GEL FOAM RESCUE MEDIAL SEPTAL NEURONS AFTER FIMBRIA FORNIX TRANSECTION, JOURNAL OF NEUROSCIENCE RESEARCH 22: 83 (1989).",
      "journal-title": "JOURNAL OF NEUROSCIENCE RESEARCH"
    },
    {
      "key": "e_1_2_1_30_1",
      "unstructured": "PAXINOS G RAT BRAIN STEREOTAXI (1986)."
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1016/0006-8993(83)90046-X",
      "volume": "289",
      "year": "1983",
      "unstructured": "PEARSON, RCA, PERSISTENCE OF CHOLINERGIC NEURONS IN THE BASAL NUCLEUS IN A BRAIN WITH SENILE DEMENTIA OF THE ALZHEIMERS TYPE DEMONSTRATED BY IMMUNOHISTOCHEMICAL STAINING FOR CHOLINE-ACETYLTRANSFERASE, BRAIN RESEARCH 289: 375 (1983).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "123",
      "DOI": "10.1038/336123a0",
      "volume": "336",
      "year": "1988",
      "unstructured": "PURVES, D, TROPHIC REGULATION OF NERVE-CELL MORPHOLOGY AND INNERVATION IN THE AUTONOMIC NERVOUS-SYSTEM, NATURE 336: 123 (1988).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3201248"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.887924"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "310",
      "DOI": "10.1016/0006-8993(87)91084-5",
      "volume": "411",
      "year": "1987",
      "unstructured": "SOFRONIEW, M.V., THE CHOLINERGIC NUCLEI OF THE BASAL FOREBRAIN OF THE RAT - NORMAL STRUCTURE, DEVELOPMENT AND EXPERIMENTALLY INDUCED DEGENERATION, BRAIN RESEARCH 411: 310 (1987).",
      "journal-title": "BRAIN RESEARCH"
    },
    {
      "key": "e_1_2_1_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "358",
      "DOI": "10.1016/0006-8993(89)91259-6",
      "volume": "476",
      "year": "1989",
      "unstructured": "Sofroniew, M. V., Brain Research 476: 358 (1989).",
      "journal-title": "Brain Research"
    },
    {
      "key": "e_1_2_1_37_1",
      "first-page": "327",
      "volume": "1",
      "year": "1988",
      "unstructured": "SOFRONIEW, M.V., J CHEM NEUROANAT 1: 327 (1988).",
      "journal-title": "J CHEM NEUROANAT"
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "crossref",
      "unstructured": "SWANSON L.W. HDB CHEM NEUROANAT 1 5 (1987).",
      "DOI": "10.1097/00152193-198701000-00003"
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1523/JNEUROSCI.08-01-00265.1988",
      "volume": "8",
      "year": "1988",
      "unstructured": "VILLEGASPEREZ, M.P., INFLUENCES OF PERIPHERAL-NERVE GRAFTS ON THE SURVIVAL AND REGROWTH OF AXOTOMIZED RETINAL GANGLION-CELLS IN ADULT-RATS, JOURNAL OF NEUROSCIENCE 8: 265 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_40_1",
      "first-page": "673",
      "volume": "14",
      "year": "1988",
      "unstructured": "VILLEGASPEREZ, M.P., SOCIETY FOR NEUROSCIENCE. ABSTRACTS 14: 673 (1988).",
      "journal-title": "SOCIETY FOR NEUROSCIENCE. ABSTRACTS"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7058341"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "crossref",
      "first-page": "403",
      "DOI": "10.1002/jnr.490200402",
      "volume": "20",
      "year": "1988",
      "unstructured": "WHITTEMORE, S.R., RAT BETA-NERVE GROWTH-FACTOR SEQUENCE AND SITE OF SYNTHESIS IN THE ADULT HIPPOCAMPUS, JOURNAL OF NEUROSCIENCE RESEARCH 20: 403 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE RESEARCH"
    },
    {
      "key": "e_1_2_1_43_1",
      "first-page": "9231",
      "volume": "83",
      "year": "1986",
      "unstructured": "WILLIAMS, L.R., CONTINUOUS INFUSION OF NERVE GROWTH-FACTOR PREVENTS BASAL FOREBRAIN NEURONAL DEATH AFTER FIMBRIA FORNIX TRANSECTION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 9231 (1986).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.1688664",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        11
      ]
    ],
    "date-time": "2024-01-11T15:23:47Z",
    "timestamp": 1704986627000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.1688664"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1990,
        1,
        19
      ]
    ]
  },
  "references-count": 43,
  "journal-issue": {
    "issue": "4940",
    "published-print": {
      "date-parts": [
        [
          1990,
          1,
          19
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.1688664"
  ],
  "URL": "http://dx.doi.org/10.1126/science.1688664",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1990,
        1,
        19
      ]
    ]
  }
}