DOI: 10.1002/ana.10078. Dopaminergic modulation of cortical function in patients with Parkinson's disease

Dopaminergic modulation of cortical function in patients with Parkinson's disease

10.1002/ana.10078

Crossref journal-article

Wiley

Annals of Neurology (311)

Abstract

AbstractPatients with idiopathic Parkinson's disease suffer not only from classic motor symptoms, but from deficits in cognitive function, primarily those subserved by the prefrontal cortex as well. The aim of the current study was to investigate the modulatory effects of dopaminergic therapy on neural systems subserving working memory and motor function in patients with Parkinson's disease. Ten patients with stage I and II Parkinson's disease were studied with functional magnetic resonance imaging, during a relatively hypodopaminergic state (ie, 12 hours after a last dose of dopamimetic treatment), and again during a dopamine‐replete state. Functional magnetic resonance imaging was performed under three conditions: a working memory task, a cued sensorimotor task and rest. Consistent with prior data, the cortical motor regions activated during the motor task showed greater activation during the dopamine‐replete state; however, the cortical regions subserving working memory displayed greater activation during the hypodopaminergic state. Interestingly, the increase in cortical activation during the working memory task in the hypodopaminergic state positively correlated with errors in task performance, and the increased activation in the cortical motor regions during the dopamine‐replete state was positively correlated with improvement in motor function. These results support evidence from basic research that dopamine modulates cortical networks subserving working memory and motor function via two distinct mechanisms: nigrostriatal projections facilitate motor function indirectly via thalamic projections to motor cortices, whereas the mesocortical dopaminergic system facilitates working memory function via direct inputs to prefrontal cortex. The results are also consistent with evidence that the hypodopaminergic state is associated with decreased efficiency of prefrontal cortical information processing and that dopaminergic therapy improves the physiological efficiency of this region.

Bibliography

Mattay, V. S., Tessitore, A., Callicott, J. H., Bertolino, A., Goldberg, T. E., Chase, T. N., Hyde, T. M., & Weinberger, D. R. (2002). Dopaminergic modulation of cortical function in patients with Parkinsonâs disease. Annals of Neurology, 51(2), 156â164. Portico.

Authors 8

Venkata S. Mattay (first)
Alessandro Tessitore (additional)
Joseph H. Callicott (additional)
Alessandro Bertolino (additional)
Terry E. Goldberg (additional)
Thomas N. Chase (additional)
Thomas M. Hyde (additional)
Daniel R. Weinberger (additional)

References 65 Referenced 319

10.1001/archneur.55.5.674
10.1016/0278-2626(90)90051-O
10.1016/0028-3932(93)90077-D
{'key': 'e_1_2_6_5_2', 'first-page': '201', 'article-title': "Does cognitive impairment in Parkinson's disease result from non‐dopaminergic lesions?", 'volume': '52', 'author': 'Pillon B', 'year': '1989', 'journal-title': 'J Neurol'} / J Neurol / Does cognitive impairment in Parkinson's disease result from non‐dopaminergic lesions? by Pillon B (1989)
10.1093/brain/111.3.525
10.1037/0894-4105.11.2.171 / Neuropsychology / Spatial, but not object delayed response is impaired in early Parkinson's disease by Postle B (1997)
10.1016/0028-3932(95)00010-Z
{'key': 'e_1_2_6_9_2', 'first-page': '125', 'article-title': 'Deficits on visuospatial tests involving forward planning in high‐functioning parkinsonians', 'volume': '3', 'author': 'Ogden J', 'year': '1990', 'journal-title': 'Neuropsychiatry Neuropsychol Behav Neurol'} / Neuropsychiatry Neuropsychol Behav Neurol / Deficits on visuospatial tests involving forward planning in high‐functioning parkinsonians by Ogden J (1990)
10.1016/0166-2236(90)90110-V / Trends Neurosci / Primate models of movement disorder of basal ganglia origin by DeLong M (1990)
10.1002/ana.410320608
10.1136/jnnp.57.5.567
10.1093/brain/123.2.394
10.1126/science.7679223
10.2165/00002512-200016050-00006
10.1093/brain/121.5.949
{'issue': '1', 'key': 'e_1_2_6_17_2', 'first-page': '168', 'article-title': "The relationship between “frontal” function in patients with Parkinson's disease and brain dopaminergic activity as measured by PET", 'volume': '40', 'author': 'Leenders K', 'year': '1990', 'journal-title': 'Neurology'} / Neurology / The relationship between “frontal” function in patients with Parkinson's disease and brain dopaminergic activity as measured by PET by Leenders K (1990)
10.1007/BF02252963
10.1016/S0304-3940(98)00928-8
10.1001/archneur.57.4.470
10.1002/1531-8249(199911)46:5<723::AID-ANA7>3.0.CO;2-R
10.1002/1531-8249(199905)45:5<601::AID-ANA8>3.0.CO;2-0
10.1146/annurev.ne.09.030186.002041
10.1212/WNL.30.12.1326
10.1016/0006-8993(83)90993-9
10.1016/0006-8993(75)90699-X
10.1016/0006-8993(76)90140-2
10.1523/JNEUROSCI.16-15-04816.1996 / J Neurosci / Dextroamphetamine enhances “neural network‐specific” physiological signals: a positron‐emission tomography rCBF study by Mattay V (1996)
10.1016/S1054-3589(08)60846-7
10.1073/pnas.98.1.301
10.1038/376572a0
10.1038/376572a0
10.1016/S0893-133X(98)00112-2
10.1111/j.1600-0404.2007.00818.x
10.1002/mrm.1910360418
10.1093/cercor/9.1.20
10.1006/nimg.2000.0610
10.1097/00004728-199709000-00029
10.1148/radiology.201.2.8888231
10.1097/00004728-199801000-00028
10.1097/00004728-199801000-00027
10.1093/cercor/10.11.1078
10.1002/cne.903250102
10.1016/S0165-0173(99)00045-4
10.1126/science.1825731
10.1016/S1353-8020(00)00044-4
10.1073/pnas.93.3.1325
10.1073/pnas.86.22.9015
10.1002/cne.903630208
{'key': 'e_1_2_6_50_2', 'first-page': '1569', 'article-title': 'Effects of neonatal hippocampal lesions in prefrontal cortical pyramidal cell responses to VTA stimulation', 'volume': '25', 'author': "O'Donnell P", 'year': '1999', 'journal-title': 'Soc Neurosci Abs'} / Soc Neurosci Abs / Effects of neonatal hippocampal lesions in prefrontal cortical pyramidal cell responses to VTA stimulation by O'Donnell P (1999)
10.1093/cercor/10.12.1168
10.1152/jn.1997.78.5.2795
10.1152/jn.1990.63.6.1385 / J Neurophysiol / Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex by Sawaguchi T (1990)
10.1152/jn.1990.63.6.1401
10.1152/jn.1987.58.5.1100 / J Neurophysiol / Catecholamine sensitivities of neurons related to a visual reaction time task in the monkey prefrontal cortex by Sawaguchi T (1987)
10.1176/jnp.1.4.377
10.1016/0304-3940(92)90345-8
10.1038/378180a0
10.1523/JNEUROSCI.11-07-01907.1991
CoolsR StefanovaE BarkerRA et al.Dopaminergic modulation of high‐level cognition in Parkinson's disease: The role of prefrontal cortex revealed by PET. In press.
10.1016/0022-510X(73)90175-5
10.1007/978-3-7091-6360-3_1
10.1002/ana.410300308
10.1523/JNEUROSCI.16-01-00373.1996 / J Neurosci / NMDA receptor antagonists impair prefrontal cortex function as assessed via apatial delayed alteration performance in rats: modulation by dopamine by Verma A (1996)
10.1016/S1364-6613(98)01240-6
10.1177/026988119701100208

Dates

Type	When
Created	23 years ago (Aug. 25, 2002, 6:17 p.m.)
Deposited	1 year, 10 months ago (Oct. 17, 2023, 10:52 a.m.)
Indexed	1 week, 2 days ago (Aug. 24, 2025, 6:49 p.m.)
Issued	23 years, 7 months ago (Jan. 31, 2002)
Published	23 years, 7 months ago (Jan. 31, 2002)
Published Online	23 years, 7 months ago (Jan. 31, 2002)
Published Print	23 years, 7 months ago (Feb. 1, 2002)

Funders 0

None

BibTeX

@article{Mattay_2002, title={Dopaminergic modulation of cortical function in patients with Parkinson’s disease}, volume={51}, ISSN={1531-8249}, url={http://dx.doi.org/10.1002/ana.10078}, DOI={10.1002/ana.10078}, number={2}, journal={Annals of Neurology}, publisher={Wiley}, author={Mattay, Venkata S. and Tessitore, Alessandro and Callicott, Joseph H. and Bertolino, Alessandro and Goldberg, Terry E. and Chase, Thomas N. and Hyde, Thomas M. and Weinberger, Daniel R.}, year={2002}, month=jan, pages={156–164} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        24
      ]
    ],
    "date-time": "2025-08-24T22:49:30Z",
    "timestamp": 1756075770771
  },
  "reference-count": 65,
  "publisher": "Wiley",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2002,
            1,
            31
          ]
        ],
        "date-time": "2002-01-31T00:00:00Z",
        "timestamp": 1012435200000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2002,
        2
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Patients with idiopathic Parkinson's disease suffer not only from classic motor symptoms, but from deficits in cognitive function, primarily those subserved by the prefrontal cortex as well. The aim of the current study was to investigate the modulatory effects of dopaminergic therapy on neural systems subserving working memory and motor function in patients with Parkinson's disease. Ten patients with stage I and II Parkinson's disease were studied with functional magnetic resonance imaging, during a relatively hypodopaminergic state (ie, 12 hours after a last dose of dopamimetic treatment), and again during a dopamine\u2010replete state. Functional magnetic resonance imaging was performed under three conditions: a working memory task, a cued sensorimotor task and rest. Consistent with prior data, the cortical motor regions activated during the motor task showed greater activation during the dopamine\u2010replete state; however, the cortical regions subserving working memory displayed greater activation during the hypodopaminergic state. Interestingly, the increase in cortical activation during the working memory task in the hypodopaminergic state positively correlated with errors in task performance, and the increased activation in the cortical motor regions during the dopamine\u2010replete state was positively correlated with improvement in motor function. These results support evidence from basic research that dopamine modulates cortical networks subserving working memory and motor function via two distinct mechanisms: nigrostriatal projections facilitate motor function indirectly via thalamic projections to motor cortices, whereas the mesocortical dopaminergic system facilitates working memory function via direct inputs to prefrontal cortex. The results are also consistent with evidence that the hypodopaminergic state is associated with decreased efficiency of prefrontal cortical information processing and that dopaminergic therapy improves the physiological efficiency of this region.</jats:p>",
  "DOI": "10.1002/ana.10078",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        8,
        25
      ]
    ],
    "date-time": "2002-08-25T22:17:27Z",
    "timestamp": 1030313847000
  },
  "page": "156-164",
  "source": "Crossref",
  "is-referenced-by-count": 319,
  "title": "Dopaminergic modulation of cortical function in patients with Parkinson's disease",
  "prefix": "10.1002",
  "volume": "51",
  "author": [
    {
      "given": "Venkata S.",
      "family": "Mattay",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Alessandro",
      "family": "Tessitore",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Joseph H.",
      "family": "Callicott",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Alessandro",
      "family": "Bertolino",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Terry E.",
      "family": "Goldberg",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Thomas N.",
      "family": "Chase",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Thomas M.",
      "family": "Hyde",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Daniel R.",
      "family": "Weinberger",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2002,
        1,
        31
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_6_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/archneur.55.5.674"
    },
    {
      "key": "e_1_2_6_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0278-2626(90)90051-O"
    },
    {
      "key": "e_1_2_6_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3932(93)90077-D"
    },
    {
      "key": "e_1_2_6_5_2",
      "first-page": "201",
      "article-title": "Does cognitive impairment in Parkinson's disease result from non\u2010dopaminergic lesions?",
      "volume": "52",
      "author": "Pillon B",
      "year": "1989",
      "journal-title": "J Neurol"
    },
    {
      "key": "e_1_2_6_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/brain/111.3.525"
    },
    {
      "key": "e_1_2_6_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "171",
      "DOI": "10.1037/0894-4105.11.2.171",
      "article-title": "Spatial, but not object delayed response is impaired in early Parkinson's disease",
      "volume": "11",
      "author": "Postle B",
      "year": "1997",
      "journal-title": "Neuropsychology"
    },
    {
      "key": "e_1_2_6_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0028-3932(95)00010-Z"
    },
    {
      "key": "e_1_2_6_9_2",
      "first-page": "125",
      "article-title": "Deficits on visuospatial tests involving forward planning in high\u2010functioning parkinsonians",
      "volume": "3",
      "author": "Ogden J",
      "year": "1990",
      "journal-title": "Neuropsychiatry Neuropsychol Behav Neurol"
    },
    {
      "key": "e_1_2_6_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "281",
      "DOI": "10.1016/0166-2236(90)90110-V",
      "article-title": "Primate models of movement disorder of basal ganglia origin",
      "author": "DeLong M",
      "year": "1990",
      "journal-title": "Trends Neurosci"
    },
    {
      "key": "e_1_2_6_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ana.410320608"
    },
    {
      "key": "e_1_2_6_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1136/jnnp.57.5.567"
    },
    {
      "key": "e_1_2_6_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/brain/123.2.394"
    },
    {
      "key": "e_1_2_6_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7679223"
    },
    {
      "key": "e_1_2_6_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.2165/00002512-200016050-00006"
    },
    {
      "key": "e_1_2_6_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/brain/121.5.949"
    },
    {
      "issue": "1",
      "key": "e_1_2_6_17_2",
      "first-page": "168",
      "article-title": "The relationship between \u201cfrontal\u201d function in patients with Parkinson's disease and brain dopaminergic activity as measured by PET",
      "volume": "40",
      "author": "Leenders K",
      "year": "1990",
      "journal-title": "Neurology"
    },
    {
      "key": "e_1_2_6_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02252963"
    },
    {
      "key": "e_1_2_6_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0304-3940(98)00928-8"
    },
    {
      "key": "e_1_2_6_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/archneur.57.4.470"
    },
    {
      "key": "e_1_2_6_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1531-8249(199911)46:5<723::AID-ANA7>3.0.CO;2-R"
    },
    {
      "key": "e_1_2_6_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1531-8249(199905)45:5<601::AID-ANA8>3.0.CO;2-0"
    },
    {
      "key": "e_1_2_6_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.ne.09.030186.002041"
    },
    {
      "key": "e_1_2_6_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1212/WNL.30.12.1326"
    },
    {
      "key": "e_1_2_6_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(83)90993-9"
    },
    {
      "key": "e_1_2_6_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(75)90699-X"
    },
    {
      "key": "e_1_2_6_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(76)90140-2"
    },
    {
      "key": "e_1_2_6_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "4816",
      "DOI": "10.1523/JNEUROSCI.16-15-04816.1996",
      "article-title": "Dextroamphetamine enhances \u201cneural network\u2010specific\u201d physiological signals: a positron\u2010emission tomography rCBF study",
      "volume": "16",
      "author": "Mattay V",
      "year": "1996",
      "journal-title": "J Neurosci"
    },
    {
      "key": "e_1_2_6_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1054-3589(08)60846-7"
    },
    {
      "key": "e_1_2_6_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.98.1.301"
    },
    {
      "key": "e_1_2_6_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/376572a0"
    },
    {
      "key": "e_1_2_6_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/376572a0"
    },
    {
      "key": "e_1_2_6_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0893-133X(98)00112-2"
    },
    {
      "key": "e_1_2_6_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-0404.2007.00818.x"
    },
    {
      "key": "e_1_2_6_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mrm.1910360418"
    },
    {
      "key": "e_1_2_6_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/cercor/9.1.20"
    },
    {
      "key": "e_1_2_6_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/nimg.2000.0610"
    },
    {
      "key": "e_1_2_6_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00004728-199709000-00029"
    },
    {
      "key": "e_1_2_6_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1148/radiology.201.2.8888231"
    },
    {
      "key": "e_1_2_6_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00004728-199801000-00028"
    },
    {
      "key": "e_1_2_6_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00004728-199801000-00027"
    },
    {
      "key": "e_1_2_6_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/cercor/10.11.1078"
    },
    {
      "key": "e_1_2_6_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.903250102"
    },
    {
      "key": "e_1_2_6_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0165-0173(99)00045-4"
    },
    {
      "key": "e_1_2_6_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1825731"
    },
    {
      "key": "e_1_2_6_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1353-8020(00)00044-4"
    },
    {
      "key": "e_1_2_6_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.3.1325"
    },
    {
      "key": "e_1_2_6_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.22.9015"
    },
    {
      "key": "e_1_2_6_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cne.903630208"
    },
    {
      "key": "e_1_2_6_50_2",
      "first-page": "1569",
      "article-title": "Effects of neonatal hippocampal lesions in prefrontal cortical pyramidal cell responses to VTA stimulation",
      "volume": "25",
      "author": "O'Donnell P",
      "year": "1999",
      "journal-title": "Soc Neurosci Abs"
    },
    {
      "key": "e_1_2_6_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/cercor/10.12.1168"
    },
    {
      "key": "e_1_2_6_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1997.78.5.2795"
    },
    {
      "key": "e_1_2_6_53_2",
      "doi-asserted-by": "crossref",
      "first-page": "1385",
      "DOI": "10.1152/jn.1990.63.6.1385",
      "article-title": "Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex",
      "volume": "63",
      "author": "Sawaguchi T",
      "year": "1990",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "e_1_2_6_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1990.63.6.1401"
    },
    {
      "key": "e_1_2_6_55_2",
      "doi-asserted-by": "crossref",
      "first-page": "1100",
      "DOI": "10.1152/jn.1987.58.5.1100",
      "article-title": "Catecholamine sensitivities of neurons related to a visual reaction time task in the monkey prefrontal cortex",
      "volume": "58",
      "author": "Sawaguchi T",
      "year": "1987",
      "journal-title": "J Neurophysiol"
    },
    {
      "key": "e_1_2_6_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1176/jnp.1.4.377"
    },
    {
      "key": "e_1_2_6_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0304-3940(92)90345-8"
    },
    {
      "key": "e_1_2_6_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/378180a0"
    },
    {
      "key": "e_1_2_6_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.11-07-01907.1991"
    },
    {
      "key": "e_1_2_6_60_2",
      "unstructured": "CoolsR StefanovaE BarkerRA et al.Dopaminergic modulation of high\u2010level cognition in Parkinson's disease: The role of prefrontal cortex revealed by PET. In press."
    },
    {
      "key": "e_1_2_6_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-510X(73)90175-5"
    },
    {
      "key": "e_1_2_6_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-3-7091-6360-3_1"
    },
    {
      "key": "e_1_2_6_63_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ana.410300308"
    },
    {
      "key": "e_1_2_6_64_2",
      "doi-asserted-by": "crossref",
      "first-page": "373",
      "DOI": "10.1523/JNEUROSCI.16-01-00373.1996",
      "article-title": "NMDA receptor antagonists impair prefrontal cortex function as assessed via apatial delayed alteration performance in rats: modulation by dopamine",
      "volume": "16",
      "author": "Verma A",
      "year": "1996",
      "journal-title": "J Neurosci"
    },
    {
      "key": "e_1_2_6_65_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1364-6613(98)01240-6"
    },
    {
      "key": "e_1_2_6_66_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/026988119701100208"
    }
  ],
  "container-title": "Annals of Neurology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fana.10078",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/ana.10078",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        17
      ]
    ],
    "date-time": "2023-10-17T14:52:31Z",
    "timestamp": 1697554351000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/ana.10078"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2002,
        1,
        31
      ]
    ]
  },
  "references-count": 65,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          2002,
          2
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/ana.10078"
  ],
  "URL": "http://dx.doi.org/10.1002/ana.10078",
  "relation": {},
  "ISSN": [
    "0364-5134",
    "1531-8249"
  ],
  "subject": [],
  "container-title-short": "Annals of Neurology",
  "published": {
    "date-parts": [
      [
        2002,
        1,
        31
      ]
    ]
  }
}