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Differential Reductions in Dopaminergic Innervation of the Motor-Related Areas of the Frontal Lobe in MPTP-Treated Monkeys

  • Yoshio Yamaji
  • Masaru Matsumura
  • Jun Kojima
  • Hironobu Tokuno
  • Atsushi Nambu
  • Masahiko Inase
  • Hisamasa Imai
  • Masahiko Takada
Part of the Advances in Behavioral Biology book series (ABBI, volume 54)

Abstract

Unexpectedly widespread dopaminergic innervation has been recognized in the primate cerebral cortex. The cortical dopaminergic fibers are distributed throughout the frontal-tooccipital extent, with the highest density in the prefrontal and motor-related areas of the frontal lobe.1-10Previous anatomical studies have shown that multiple motor-related areas of the frontal lobe, such as the primary motor cortex (MI), the premotor cortex (PM), and the supplementary motor area (SMA), contain dopaminergic fibers.1–3,7,8,10 The dopaminergic innervation of the motor-related areas is diffuse, involving all cortical layers.3,7,8,10 On the other hand, the cortical dopaminergic fibers as a whole arise from the three catecholaminergic cell groups—A8, A9, and A 10—that are located in the ventral mesencephalon.3 It has been reported that the cells of origin of the mesocortical dopamine projections to the dorsal frontal cortex, including the motor-related areas, are distributed predominantly in the dorsal aspects of the A8–A10 complex.11,12 In primates, the dorsal components of these catecholaminergic cell groups largely correspond to the dorsal part of the retrorubral area, pars gamma (i e, the dorsal tier) of the substantia nigra pars compacta, and the parabrachial pigmented nucleus of the ventral tegmental area, respectively. Given that subpopulations of dopaminergic neurons in such dorsal components may issue axon collaterals to both the frontal cortex and the striatum (for data in the rat, see refs.13,15), it is most likely that at least part of the dopaminergic fibers in the motor-related areas are affected in Parkinson’s disease which is well known to be caused by the extensive loss of dopaminergic nigrostriatal neurons.

Keywords

Ventral Tegmental Area Supplementary Motor Area Primary Motor Cortex Ventral Mesencephalon Immunoreactive Fiber 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Berger, B., Trottier, S., Gaspar, P., Verney, C., and Alvarez, C., 1986, Major dopamine innervation of the cortical motor areas in theCynomolgusmonkey. A radioautographic study with comparative assessment of serotonergic afferentsNeurosci. Lett.72:121–127.PubMedCrossRefGoogle Scholar
  2. 2.
    Berger, B., Trottier, S., Verney, C., Gaspar, P., and Alvarez, C., 1988, Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: A radioautographic studyJ. Comp. Neurol.273:99–119.PubMedCrossRefGoogle Scholar
  3. 3.
    Berger, B., Gaspar, P., and Verney, C., 1991, Dopaminergic innervation of the cerebral cortex: Unexpected differences between rodents and primatesTrends Neurosci.14:21–27.PubMedCrossRefGoogle Scholar
  4. 4.
    Björklund, A., Divac, I., and Lindvall, O., 1978, Regional distribution of catecholamines in monkey cerebral cortex, evidence for a dopaminergic innervation of the primate prefrontal cortexNeurosci. Lett.7:115–119.PubMedCrossRefGoogle Scholar
  5. 5.
    Brown, R.M., Crane, A.M., and Goldman, P.S., 1979, Regional distribution of monoamines in the cerebral cortex and subcortical structures of the rhesus monkey: Concentrations and in vivo synthesis ratesBrain Res.168:133–150.PubMedCrossRefGoogle Scholar
  6. 6.
    De Keyser, J., Ebinger, G, and Vauquelin, G., 1989, Evidence for a widespread dopaminergic innervation of the human cerebral neocortexNeurosci. Lett.104:281–285.PubMedCrossRefGoogle Scholar
  7. 7.
    Gaspar, P., Berger, B., Febvret, A., Vigny, A., and Henry, J.P., 1989, Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-beta-hydroxylaseJ. Comp. Neurol.279:249–271.PubMedCrossRefGoogle Scholar
  8. 8.
    Gaspar, P., Duyckaerts, C., Alvarez, C., Javoy-Agid, F., and Berger, B., 1991, Alterations of dopaminergic and noradrenergic innervations in motor cortex in Parkinson’s diseaseAnn. Neurol.30:365–374.PubMedCrossRefGoogle Scholar
  9. 9.
    Levitt, P., Rakic, P., and Goldman-Rakic, P., 1984, Region-specific distribution of catecholamine afferents in primate cerebral cortex: A fluorescence histochemical analysisJ. Comp. Neurol.227:2336.CrossRefGoogle Scholar
  10. 10.
    Lewis, D.A., Campbell, M.J., Foote, S.L., Goldstein, M., and Morrison, J.H., 1987, The distribution of tyrosine hydroxylase-immunoreactive fibers in primate neocortex is widespread but regionally specificJ. Neurosci.7:279–290.PubMedGoogle Scholar
  11. 11.
    Gaspar, P., Stepniewska, I., and Kaas, J.H., 1992, Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys, J.Comp. Neurol.325:1–21.PubMedCrossRefGoogle Scholar
  12. 12.
    Williams, S.M., and Goldman-Rakic, P.S., 1998, Widespread origin of the primate mesofrontal dopamine systemCereb. Cortex8:321–345.PubMedCrossRefGoogle Scholar
  13. 13.
    Fallon, J.H., and Loughlin, S.E., 1982, Monoamine innervation of the forebrain: CollateralizationBrain Res. Bull.9:295–307.PubMedCrossRefGoogle Scholar
  14. 14.
    Loughlin, S.E., and Fallon, J.H., 1984, Substantia nigra and ventral tegmental area projections to cortex: Topography and collateralizationNeuroscience11:425–435.PubMedCrossRefGoogle Scholar
  15. 15.
    Takada, M., and Hattori, T., 1986, Collateral projections from the substantia nigra to the cingulate cortex and striatum in therat Brain Res.380:331–335.PubMedCrossRefGoogle Scholar
  16. 16.
    Elsworth, J.D., Deutch, A.Y., Redmond, D.E., Jr., Sladek, J.R., Jr., and Roth, R.H., 1990, MPTP reduces dopamine and norepinephrine concentrations in the supplementary motor area and cingulate cortex of the primateNeuroscd. Lett.114:316–322.CrossRefGoogle Scholar
  17. 17.
    Damier, P., Hirsch, E.C., Agid, Y., and Graybiel, A.M., 1999, The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D28K immunohistochemistryBrain 122:1421–1436.PubMedCrossRefGoogle Scholar
  18. 18.
    Damier, P., Hirsch, E.C., Agid, Y., and Graybiel, A.M., 1999, The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s diseaseBrain122:1437–1448.PubMedCrossRefGoogle Scholar
  19. 19.
    German, D.C., Manaye, K.F., Sonsalla, P.K., and Brooks, B.A., 1992, Midbrain dopaminergic cell loss in Parkinson’s disease and MPTP-induced parkinsonism: Sparing of calbindin-D28-containing cellsAnn. N. Y. Acad. Sci.648:42–62.Google Scholar
  20. 20.
    Lavoie, B., and Parent, A., 1991, Dopaminergic neurons expressing calbindin in normal and parkinsonian monkeysNeuroreport2:601–604.PubMedCrossRefGoogle Scholar
  21. 21.
    Yamada, T., McGeer, P.L., Baimbridge, K.G, and McGeer, E.G, 1990, Relative sparing in Parkinson’s disease of substanfia nigra dopamine neurons containing calbindin-DBK Brain Res.526:303–307.PubMedCrossRefGoogle Scholar
  22. 22.
    Picard, N., and Strick, P.L., 1996, Motor areas of the medial wall: A review of their location and functional activationCereb. Cortex6:342–353.PubMedCrossRefGoogle Scholar
  23. 23.
    Tanji, J., 1994, The supplementary motor area in the cerebral cortexNeurosci. Res.19:251–268.PubMedCrossRefGoogle Scholar
  24. 24.
    Inase, M., Tokuno, H., Nambu, A., Akazawa, T., and Takada, M., 1999, Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: Comparison with the input zones from the supplementary motor areaBrain Res.833:191–201.PubMedCrossRefGoogle Scholar
  25. 25.
    Nambu, A., Takada, M., Inase, M., and Tokuno, H., 1996, Dual somatotopical representations in the primate subthalamic nucleus: Evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor areaJ. Neurosci.16:2671–2683.PubMedGoogle Scholar
  26. 26.
    Takada, M., Tokuno, H., Nambu, A., and Inase, M., 1998, Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: Segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortexExp. Brain Res.120:114–128.PubMedCrossRefGoogle Scholar
  27. 27.
    Herkenham, M., Little, M.D., Bankiewicz, K., Yang, S.-C., Markey, S.P., and Johannessen, J.N., 1991, Selective retention of MPP+ within the monoaminergic systems of the primate brain following MPTP administration: Anin vivoautoradiographic studyNeuroscience40:133–158.PubMedCrossRefGoogle Scholar
  28. 28.
    Deutch, A.Y., Elsworth, J.D., Goldstein, M., Fuxe, K., Redmond, D.E., Jr., Sladek, J.R., Jr., and Roth, R.H., 1986, Preferential vulnerability of A8 dopamine neurons in the primate to the neurotoxin 1methyl-4-phenyl-1,2,3,6-tetrahydropyridineNeurosci. Lett.68:51–56.PubMedCrossRefGoogle Scholar
  29. 29.
    Elsworth, J.D., Deutch, A.Y., Redmond, D.E., Jr., Sladek, J.R., Jr., and Roth, R.H., 1990, MPTPinduced parkinsonism: relative changes in dopamine concentration in subregions of substantia nigra, ventral tegmental area and retrorubral field of symptomatic and asymptomatic vervet monkeysBrain Res.513:320–324.PubMedCrossRefGoogle Scholar
  30. 30.
    German, D.C., Dubach, M., Askari, S., Speciale, S.G, and Bowden, D.M., 1988, 1-methyl-4phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonian syndrome inMacaca fascicularis:Which midbrain dopaminergic neurons are lost?Neuroscience24:161–174.PubMedCrossRefGoogle Scholar
  31. 31.
    Kastner, A., Hirsch, E.C., Herrero, M.T., Javoy-Agid, F., and Agid, Y., 1993, Immunocytochemical quantification of tyrosine hydroxylase at a cellular level in the mesencephalon of control subjects and patients with Parkinson’s and Alzheimer’s diseaseJ. Neurochem.61:1024–1034.PubMedCrossRefGoogle Scholar
  32. 32.
    Palombo, E., Porrino, L.J., Bankiewicz, K.S., Crane, A.M., Sokoloff, L., and Kopin, I.J., 1990, Local cerebral glucose utilization in monkeys with hemiparkinsonism induced by intracarotid infusion of the neurotoxin MPTPJ. Neurosci.10:860–869.PubMedGoogle Scholar
  33. 33.
    Brinkman, C., 1984, Supplementary motor area of the monkey’s cerebral cortex: Short-and longterm deficits after unilateral ablation and the effects of subsequent callosal sectionJ. Neurosci.4:918–929.PubMedGoogle Scholar
  34. 34.
    Cunnington, R., Iansek, R., Bradshaw, J.L., and Phillips, J.G., 1995, Movement-related potentials in Parkinson’s disease. Presence and predictability of temporal and spatial cuesBrain118:935–950.PubMedCrossRefGoogle Scholar
  35. 35.
    Dick, J.P., Benecke, R., Rothwell, J.C., Day, B.L., and Marsden, C.D., 1986, Simple and complex movements in a patient with infarction of the right supplementary motor areaMov. Dis.1:255–266.CrossRefGoogle Scholar
  36. 36.
    Jahanshahi, M., Jenkins, I.H., Brown, R.G., Marsden, C.D., Passingham, R.E., Brooks, D.J., 1995, Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and.movement-related potentials in normal and Parkinson’s disease subjectsBrain118:913–933.PubMedCrossRefGoogle Scholar
  37. 37.
    Jones, D.L., Phillips, J.G., Bradshaw, J.L., Lansek, R., and Bradshaw, J.A., 1992, Impairment in bilateral alternating movements in Parkinson’s disease?J. Neurol. Neurosurg. Psychiat.55:503–506.PubMedCrossRefGoogle Scholar
  38. 38.
    Praamstra, P., Cools, A.R., Stegeman, D.F., and Horstink, M.W.I.M., 1996, Movement-related potential measures of different modes of movement selection in Parkinson’s diseaseJ. Neurol. Sci.140:67–74.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Yoshio Yamaji
    • 2
  • Masaru Matsumura
    • 3
  • Jun Kojima
    • 4
  • Hironobu Tokuno
    • 1
    • 7
  • Atsushi Nambu
    • 1
    • 7
  • Masahiko Inase
    • 5
  • Hisamasa Imai
    • 6
  • Masahiko Takada
    • 1
    • 7
  1. 1.Tokyo Metropolitan Institute for NeuroscienceFuchu, TokyoJapan
  2. 2.Department of Public HealthJuntendo University School of MedicineTokyoJapan
  3. 3.Department of NeurosurgeryGunma University School of MedicineMaebashi, GunmaJapan
  4. 4.Department of NeurologySayama Neurology HospitalSayama, SaitamaJapan
  5. 5.Department of PhysiologyKinki University School of MedicineOsaka-SayamaJapan
  6. 6.Department of NeurologyJuntendo University School of MedicineTokyoJapan
  7. 7.CRESTJST (Japan Science and Technology)Japan

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