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Distinctive Chemoanatomical and Developmental Features of the Prefrontal Dopaminergic System in Primates as Compared to Rodents

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Motor and Cognitive Functions of the Prefrontal Cortex

Part of the book series: Research and Perspectives in Neurosciences ((NEUROSCIENCE))

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Abstract

Phylogenetic considerations of the dopaminergic (DA) innervation of the prefrontal cortex illustrate the pitfalls of extrapolating data obtained in rodent brain to human or nonhuman primates, as has been the case for about 15 years. Comparative studies of prefrontal DA innervation in rats and primates are complicated by several features; including the lack in rodents of a frontal area strictly homologous to the primate prefrontal cortex, the heterogeneity of the dopaminergic population which provides the cortical projections in rats, and the major evolutionary changes of the cortical DA innervation in primates. The main distinctive features between rats and primates with respect to prefrontal DA innervation are reviewed in this paper, and the value of the rat as a representative model for that study is further discussed.

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References

  • Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496

    Article  PubMed  CAS  Google Scholar 

  • Baleydier C, Mauguière F (1980) The duality of the cingulate gyrus in monkey: neuroanatomical study and functional hypothesis. Brain 103:525–554

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Haswell Henion TH, Dermon CR (1991) Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 313:65–94

    Article  PubMed  CAS  Google Scholar 

  • Bean AJ, Roth RH (1991) Extracellular dopamine and neurotensin in rat prefrontal cortex in vivo. Effects of median forebrain bundle stimulation frequency, stimulation pattern and dopamine autoreceptors. J Neurosci 11:2694–2702

    PubMed  CAS  Google Scholar 

  • Bean AJ, Dagerlind A, Hökfelt T, Dobner PR (1992) Cloning of human neurotensin/neuromedin N genomic sequences and expression in the ventral mesencephalon of schizophrenics and age/sex matched controls. Neuroscience 50:259–269

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Thierry AM, Tassin JP, Moyne MA (1976) Dopaminergic innervation of the rat prefrontal cortex: a fluorescence histochemical study. Brain Res 106:133–145

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Vemey C, Alvarez C, Vigny A, Helle KB (1985a) New dopaminergic terminal fields in the motor, visual (area 18b) and retrosplenial cortex in the young and adult rat. Immuno- cytochemical and catecholamine histochemical analyses. Neuroscience 15:983–998

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Verney C, Febvret A, Vigny A, Helle KB (1985b) Postnatal ontogenesis of the dopaminergic innervation in the rat anterior cingulate cortex (area 24). Immunocytochemical and catecholamine fluorescence histochemical analysis. Dev Brain Res 21:31–47

    Article  CAS  Google Scholar 

  • Berger B, Verney C, Gaspar P, Febvret A (1985c) Transient expression of tyrosine hydroxylase immunoreactivity in some neurons of the rat neocortex during postnatal development. Dev Brain Res 23:141–144

    Article  CAS  Google Scholar 

  • Berger B, Trottier S, Gaspar P, Verney C, Alvarez C (1986) Major dopamine innervation of the cortical motor areas in the cynomolgus monkey. A radioautographic study with comparative assessment of serotoninergic afferents. Neurosci Let 72:121–127

    Article  CAS  Google Scholar 

  • Berger B, Trottier S, Verney C, Gaspar P, Alvarez C (1988) Regional and laminar distribution of the dopamine and serotonin innervation in macaque cerebral cortex. A radioautographic study. J Comp Neurol 273:99–119

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Febvret A, Greengard P, Goldman-Rakic PS (1990) DARPP-32, a phosphoprotein enriched in dopaminoceptive neurons bearing dopamine D1 receptors: distribution in the cerebral cortex of the newborn and adult rhesus monkey. J Comp Neurol 299:327–348

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. TINS 14:21–27

    PubMed  CAS  Google Scholar 

  • Berger B, Verney C, Goldman-Rakic PS (1992) Prenatal monoaminergic innervation of the cerebral cortex; differences between rodents and primates. In: Kostovic I, Knezevic S, Spilich G (eds) Neurodevelopment, aging and cognition. Birkhauser, Boston, pp 18–36

    Google Scholar 

  • Bouthenet ML, Souil E, Martres MP, Sokoloff P, Giros B, Schwartz JC (1991) Localization of dopamine D3 receptor mRNA in the rat brain using in situ hybridization histochemistry: comparison with dopamine D2 receptor mRNA. Brain Res 564:203–219

    Article  PubMed  CAS  Google Scholar 

  • Brozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205:929–932

    Article  PubMed  CAS  Google Scholar 

  • Cepeda C, Radisavljevic Z, Peacock W, Levine MS, Buchwald NA (1992) Differential modulation by dopamine of responses evoked by excitatory aminoacids in human cortex. Synapse 11:330–341

    Article  PubMed  CAS  Google Scholar 

  • Civelli O, Bunzow JR, Grandy DK, Zhou QY, Van Tol HHM (1991) Molecular biology of the dopamine receptors. Eur J Pharmacol 207:277–286

    Article  PubMed  CAS  Google Scholar 

  • Clark FM, Proudfit HK (1992) Anatomical evidence for genetic differences in the innervation of the rat spinal cord by noradrenergic locus coeruleus neurons. Brain Res 591:44–53

    Article  PubMed  CAS  Google Scholar 

  • De Keyser J, Ebinger G, Vauquelin G (1989) Evidence for a widespread dopaminergic innervation of the human cerebral cortex. Neurosci Lett 104:281–285

    Article  PubMed  Google Scholar 

  • Descarries L, Lemay B, Doucet G, Berger B (1987) Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 21:807–824

    Article  PubMed  CAS  Google Scholar 

  • Deutch AY, Goldstein M, Baldino F, Roth RH (1988) Telencephalic projections of the A8 dopamine cell group. In: Mesocorticolimbic dopamine system. Ann NY Acad Sci 537:27–50

    Article  PubMed  CAS  Google Scholar 

  • Deutch AY, Clark WA, Roth RH (1990) Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress. Brain Res 521:311–315

    Article  PubMed  CAS  Google Scholar 

  • Dubach M, Schmidt R, Kunkel D, Bowden DM, Marti R, German DC (1987) Primate neostriatal neurons containing tyrosine hydroxylase: immunohistochemical evidence. Neurosci Lett 75:205–210

    Article  PubMed  CAS  Google Scholar 

  • Fallon JH, Loughlin SE (1987) Monoamine innervation of cerebral cortex and a theory of the role of monoamines in cerebral cortex and basal ganglia. In: Jones EG, Peters A (eds) Cerebral cortex. Vol 6. Plenum Press, New York, pp 41–127

    Google Scholar 

  • Febvret A, Berger B, Gaspar P, Verney C (1991) Further indication that distinct dopaminergic subsets project to the rat cerebral cortex: lack of colocalization with neurotensin in the superficial dopaminergic fields of the anterior cingulate, motor, retrosplenial and visual cortices. Brain Res 547:37–52

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Berger B, Febvret A, Vigny A, Krieger-Poulet M, Borri-Voltattorni C (1987) Tyrosine hydroxylase immunoreactive neurons in the human cerebral cortex: a novel cate- cholaminergic group? Neurosci Lett 80:257–262

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Berger B, Febvret A, Vigny A, Henry JP (1989) Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-β-hydroxylase. J Comp Neurol 279:249–271

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Berger B, Febvret A (1990) Neurotensin innervation of the human cerebral cortex: lack of colocalization with catecholamines. Brain Res 530:181–195

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Duyckaerts C, Alvarez C, Javoy-Agid F, Berger B (1991) Alterations of dopaminergic and noradrenergic innervations in motor cortex in Parkinson’s disease. Ann Neurol 30:365–374

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Stepniewska I, Kaas J (1992) Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in Owl monkeys. J Comp Neurol 325:1–21

    Article  PubMed  CAS  Google Scholar 

  • German DC, Manaye K, Smith WK, Woodward DJ, Saper CB (1989) Midbrain dopaminergic cell loss in Parkinson’s disease: computer visualization. Ann Neurol 26:597–514

    Article  Google Scholar 

  • Godbout R, Mantz J, Pirot S, Glowinski J, Thierry AM (1991) Inhibitory influence of the mesocortical dopaminergic neurons on their target cells: electrophysiological and pharmacological characterization. J Pharmacol Exp Therap 258:728–738

    CAS  Google Scholar 

  • Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Plum F, Mountcastle V (eds) Handbook of physiology. Bethesda, MD, American Physiol Soc, Vol 5, 373–417

    Google Scholar 

  • Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal (MD) nucleus and its projections to the frontal lobe. J Comp Neurol 242:535–560

    Article  PubMed  CAS  Google Scholar 

  • Goldman-Rakic PS, Leranth C, Williams SM, Mons N, Geffard M (1989) Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc Natl Acad Sci 86:9015–9019

    Article  PubMed  CAS  Google Scholar 

  • Goldman-Rakic PS, Lidow MS, Gallager DW (1990) Overlap of dopaminergic, adrenergic and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex. J Neurosci 10:2125–2139

    PubMed  CAS  Google Scholar 

  • Grandy DK, Zhang Y, Bouvier C, Zhou QY, Johnson RA, Allen L, Buck K, Bunzow JR, Salon J, Civelli O (1991) Multiple human D5 dopamine receptor genes: a functional receptor and two pseudogenes. Proc Nat Acad Sci 88:9175–9179

    Article  PubMed  CAS  Google Scholar 

  • Halliday GM, Törk I (1986) Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human. J Comp Neurol 52(4):423–445

    Article  Google Scholar 

  • Hara Y, Shiosaka S, Senba E, Sakanaka A, Inagaki S, Takagi H, Kawai Y, Takatsuki K, Matsuzaki T, Tohyama M (1982) Ontogeny of the neurotensin-containing neuron system of the rat: immunohistochemical analysis. 1 forebrain and diencephalon. J Comp Neurol 208:177–195

    Article  PubMed  CAS  Google Scholar 

  • Hemmings HC, Walaas SI, Ouimet CC, Greengard P (1987) Dopaminergic regulation of protein phosphorylation in the striatum: DARPP 32. TINS 10:377–383

    CAS  Google Scholar 

  • Hoffman MA (1985) Size and shape of the cerebral cortex in mammals. 1. The cortical surface. Brain Behav Evol 27:28–40

    Article  Google Scholar 

  • Hornung JP, Törk I, Detribolet N (1989) Morphology of tyrosine hydroxylase immunoreactive neurons in the human cerebral cortex. Exp Brain Res 76:12–20

    Article  PubMed  CAS  Google Scholar 

  • Huntley GW, Morrison JH, Prikhozhan A, Sealfon SC (1992) Localization of multiple dopamine receptor subtype messenger RNAs in human and monkey motor cortex and striatum. Mol Brain Res 15:181–188

    Article  PubMed  CAS  Google Scholar 

  • Iacovitti L, Lee J, Joh TH, Reis DJ (1987) Expression of tyrosine hydroxylase in neurons of cultured cerebral cortex: evidence for phenotypic plasticity in neurons of the CNS. J Neurosci 74:1264–1270

    Google Scholar 

  • Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings MBM (1988) Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 269:58–72

    Article  PubMed  CAS  Google Scholar 

  • Köhler C, Everitt BJ, Pearson J, Goldstein M (1983) Immunohistochemical evidence for a new group of catecholamine containing neurons in the basal forebrain of the monkey. Neurosci Lett 37:161–166

    Article  PubMed  Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 17:157–192

    Article  Google Scholar 

  • Kuljis RO, Martin-Vasallo P, Peress NS (1989) Lewy bodies in tyrosine hydroxylase-synthesizing neurons of the human cerebral cortex. Neurosci Lett 106:49–54

    Article  PubMed  CAS  Google Scholar 

  • Leonard CM (1969) The prefrontal cortex of the rat. 1. Cortical projection of the mediodorsal nucleus. 2. Efferent connections. Brain Res 12:321–343

    Article  PubMed  CAS  Google Scholar 

  • Lewis DA, Campbell MJ, Foote SL, Goldstein M, Morrison JH (1987) The distribution of tyrosine hydroxylase immunoreactive fibers in primate neocortex is widespread but regionally specific. J Neurosci 7:279–290

    PubMed  CAS  Google Scholar 

  • Lewis DA, Foote SL, Golstein M, Morrison JH (1988a) The dopaminergic innervation of monkey prefrontal cortex: a tyrosine hydroxylase immunohistochemical study. Brain Res 449:225–243

    Article  PubMed  CAS  Google Scholar 

  • Lewis DA, Morrison JH, Goldstein M (1988b) Brainstem dopaminergic neurons project to monkey parietal cortex. Neurosci Lett 86:11–16

    Article  PubMed  CAS  Google Scholar 

  • Lewis DA, Melchitzky DS, Gioio A, Solomon Z, Kaplan BB (1991) Neuronal localization of tyrosine hydroxylase gene products in human neocortex. Mol Cell Neurosci 2:228–234

    Article  PubMed  CAS  Google Scholar 

  • Lindvall O, Björklund A, Divac I (1978) Organization of catecholamine neurons projecting to the frontal cortex in the rat. Brain Res 142:1–24

    Article  PubMed  CAS  Google Scholar 

  • Louilot A, Taghzouti K, Simon H, Le Moal M (1989) Limbic system, basal ganglia and dopaminergic neurons. Executive and regulatory neurons and their role in the organization of behavior. Brain Behav Evol 33:157–161

    Article  PubMed  CAS  Google Scholar 

  • Marin-Padilla M (1984) Neurons of Layer I. A developmental analysis. In: Peters A and Jones EG ed. Cerebral cortex, Vol 1, Plenum Press, New York, pp 447–478

    Google Scholar 

  • Meador-Woodruff JH, Mansour A, Grandy DK, Damask SP, Civelli O, Watson Jr SJ (1992) Distribution of D5 dopamine receptor mRNA in rat brain. Neurosci Lett 145:209–212

    Article  PubMed  CAS  Google Scholar 

  • Mufson EJ, Mesulam MM (1984) Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus. J Comp Neurol 227:109–120

    Article  PubMed  CAS  Google Scholar 

  • Oeth KM, Lewis DA (1992) Cholecystokinin- and dopamine-containing mesencephalic neurons provide distinct projections to monkey prefrontal cortex. Neurosci Lett 145:87–92

    Article  PubMed  CAS  Google Scholar 

  • Ouimet CC, Miller PE, Hemmings HC, Walaas SJ, Greengard P (1984) DARPP-32, a dopamine and adenosine 3′5′monophosphate regulated phosphoprotein enriched in dopamine- innervated brain regions. III. Immunocytochemical localization. J Neurosci 4:111–124

    PubMed  CAS  Google Scholar 

  • Palacios JM, Savasta M, Mengod G (1989) Does cholecystokinin colocalize with dopamine in the human substantia nigra? Brain Res 488:369–375

    Article  PubMed  CAS  Google Scholar 

  • Park JK, Job TH, Ebner FF (1986) Tyrosine hydroxylase is expressed by neocortical neurons after transplantation. Proc Natl Acad Sci 83:7495–7498

    Article  PubMed  CAS  Google Scholar 

  • Porrino LJ, Goldman-Rakic PS (1982) Brainstem innervation of prefrontal and anterior cingulate cortex in the rhesus monkey revealed by retrograde transport of HRP. J Comp Neurol 205:63–76

    Article  PubMed  CAS  Google Scholar 

  • Retaux S, Besson MJ, Penit-Soria J (1991) Synergism between D1 and D2 dopamine receptors in the inhibition of the evoked release of H3 gaba in the rat prefrontal cortex. Neuroscience 43:323–330

    Article  PubMed  CAS  Google Scholar 

  • Richfield EK, Young AB, Penney JB (1989) Comparative distributions of dopamine D1 and D2 receptors in the cerebral cortex of rats, cats and mokeys. J Comp Neurol 286:409–426

    Article  PubMed  CAS  Google Scholar 

  • Satoh J, Suzuki K (1990) Tyrosine hydroxylase-immunoreactive neurons in the mouse cerebral cortex during the postnatal period. Dev Brain Res 53:1–5

    Article  CAS  Google Scholar 

  • Satoh H, Matsumura H (1990) Distribution of neurotensin-containing fibers in the frontal cortex of the macaque monkey. J Comp Neurol 298:215–223

    Article  PubMed  CAS  Google Scholar 

  • Sawaguchi T, Goldman-Rakic PS (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251:947–950

    Article  PubMed  CAS  Google Scholar 

  • Schalling M, Friberg K, Seroogy K, Riederer P, Bird E, Schiffman SN, Mailleux P, Vand- erhaeghen JJ, Kuga S, Goldstein M, Kitahama K, Luppi PH, Jouvet M, Hökfelt T (1990) Analysis of expression of cholecystokinin in dopamine cells in the ventral mesencephalon of several species and in humans with schizophrenia. Proc Natl Acad Sci 87:8427–8431

    Article  PubMed  CAS  Google Scholar 

  • Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560

    PubMed  CAS  Google Scholar 

  • Seguela P, Watkins KC, Descarries L (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat. Brain Res 442:11–22

    Article  PubMed  CAS  Google Scholar 

  • Seroogy KB, Dangaran K, Lim S, Haycock JW, Fallon JH (1989) Ventral mesencephalon neurons containing both cholecystokinin and tyrosine hydroxylase-like immunoreactivities project to forebrain regions. J Comp Neurol 279:397–414

    Article  PubMed  CAS  Google Scholar 

  • Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8:4049–4068

    PubMed  CAS  Google Scholar 

  • Simon H, Scatton B, Le Moal M (1980) Dopaminergic A10 neurons are involved in cognitive functions. Nature 286:150–151

    Article  PubMed  CAS  Google Scholar 

  • Smiley JF, Williams SM, Szigeti K, Goldman-Rakic PS (1992) Light and electron microscopic charecterization of dopamine immunoreactive axons in human cerebral cortex. J Comp Neurol 321:325–336

    Article  PubMed  CAS  Google Scholar 

  • Stratford TR, Wirtshafter D (1990) Ascending dopaminergic projections from the dorsal raphe nucleus in the rat. Brain Res 511:173–176

    Article  PubMed  CAS  Google Scholar 

  • Studier JM, Kitabgi P, Tramu G, Herve D, Glowinski J, Tassin JP (1988) Extensive colocalisation of neurotensin with dopamine in rat meso-cortico-frontal dopaminergic neurons. Neuropeptides 11:95–100

    Article  Google Scholar 

  • Taghzouti K, Simon H, Herve D, Blanc G, Studier JM, Glowinski J, Le Moal M, Tassin JP (1988) Behavioural deficits induced by an electrolytic lesion of the rat ventral mesencephalic tegmentum are corrected by a superimposed lesion of the dorsal noradrenergic system. Brain Res 440:172–176

    Article  PubMed  CAS  Google Scholar 

  • Thal LJ, Laing K, Horowitz SG, Makman MH (1986) Dopamine stimulates rat cortical somatostatin release. Brain Res 372:205–209

    Article  PubMed  CAS  Google Scholar 

  • Thierry AM, Blanc G, Sobel A, Stinus L, Glowinski J (1973) Dopaminergic terminals in the rat cortex. Science 182:499–501

    Article  PubMed  CAS  Google Scholar 

  • Trottier S, Geffard M, Evrard B (1989) Co-localization of tyrosine hydroxylase and gaba immunoreactivities in human cortical neurons. Neurosci Lett 106:76–82

    Article  PubMed  CAS  Google Scholar 

  • Van Eden CG, Hoorneman EMD, Buijs RM, Matthissen MAH, Geffard M, Uylings HBM (1987) Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electronmicroscopic level. Neuroscience 22:849–862

    Article  PubMed  Google Scholar 

  • Van Eden CG, Lamme VAF, Uylings HBM (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur J Neurosci 4:77–97

    Article  PubMed  Google Scholar 

  • Van Tol HHM, Bunzow JR, Guan HC, Sunahara RK, Seeman P, Niznik HB, Civelli O (1991) Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine. Nature 350:610–614

    Article  PubMed  Google Scholar 

  • Verney C, Berger B, Adrien J, Vigny A, Gay M (1982) Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using antityrosine hydroxylase antibodies. Dev Brain Res 5:41–52

    Article  Google Scholar 

  • Verney C, Alvarez C, Geffard M, Berger B (1990) Ultrastructural double labeling study of dopamine terminals and gaba-containing neurons in rat anteromedial cerebral cortex. Eur J Neurosci 2:960–972

    Article  PubMed  Google Scholar 

  • Vincent SR, Hope BT (1990) Tyrosine hydroxylase containing neurons lacking aromatic amin- oacid decarboxylase in the hamster brain. J Comp Neurol 295:290–298

    Article  PubMed  CAS  Google Scholar 

  • Yang CR, Mogenson GJ (1990) Dopaminergic modulation of cholinergic responses in rat medial prefrontal cortex. An electrophysiological study. Brain Res 524:271–281

    Article  PubMed  CAS  Google Scholar 

  • Yoshida M, Shirouzu M, Tanaka M, Semba K, Fibiger HC (1989) Dopaminergic neurons in the nucleus raphe dorsalis innervate the prefrontal cortex in the rat: a combined retrograde tracing and immunohistochemical study using antidopamine serum. Brain Res 496:373–376

    Article  PubMed  CAS  Google Scholar 

  • Zecevic N, Verney C, Milosevic A, Berger B (1991) First description of the central catecholamine systems in 6–8 week-old human embryos. Soc Neurosci Abst 17:745

    Google Scholar 

  • Zhu ZQ, Armstrong DL, Grossman RG, Hamilton WJ (1990) Tyrosine hydroxylase- immunoreactive neurons in the temporal lobe in complex partial seizures. Ann Neurol 27:564–572

    Article  PubMed  CAS  Google Scholar 

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Berger, B. (1994). Distinctive Chemoanatomical and Developmental Features of the Prefrontal Dopaminergic System in Primates as Compared to Rodents. In: Thierry, A.M., Glowinski, J., Goldman-Rakic, P.S., Christen, Y. (eds) Motor and Cognitive Functions of the Prefrontal Cortex. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-85007-3_2

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