Skip to main content
SpringerLink
Log in

Layer-specific innervation of the dopamine-deficient frontal cortex in weaver mutant mice by grafted mesencephalic dopaminergic neurones

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The dopamine innervation of the frontal cortex originates in the A9 and A10 mesencephalic dopamine cell groups. In weaver mutant mice, there is a 77% frontocortical dopamine deficiency associated with losses of dopamine neurones in areas A9 and A10. The dopamine-depleted cortical areas of weaver mutant mice are receptive to reinnervation by afferent fibres originating in dopamine-containing mesencephalic grafts from normal donor embryos. In the anteromedial frontal lobe, reinnervation by tyrosine hydroxylase immunoreactive fibres is largely confined to the basal cortical layers whereas in the anterior cingulate cortex, tyrosine hydroxylase immunoreactive fibres also occupy superficial layers, including the molecular layer. Normally, the dopaminergic innervation of the anteromedial frontal lobe is distributed among the basal cortical layers (IV–VI), and the dopaminergic innervation of the cingulate cortex occupies both basal and superficial cortical layers. The pattern of innervation following transplantation indicates that, in repopulating dopamine-deficient cortical areas of recipient weaver mutants, graft-derived dopamine fibres show a preference for those layers which are normally invested by dopamine afferents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Attardi DG, Sperry RW (1963) Preferential selection of central pathways by regenerating optic fibers. Exp Neurol 7:46–64

    Google Scholar 

  • Björklund A, Lindvall O (1984) Dopamine-containing systems in the CNS. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 2. Elsevier, Amsterdam New York Oxford, pp 55–122

    Google Scholar 

  • Björklund A, Stenevi U (1977) Reformation of the severed septohippocampal cholinergic pathway in the adult rat by transplanted septal neurons. Cell Tissue Res 185:289–302

    Google Scholar 

  • Björklund A, Stenevi U, Svendgaard N-A (1976) Growth of transplanted monoaminergic neurones into the adult hippocampus along the perforant path. Nature (Lond) 262:787–790

    Google Scholar 

  • Björklund A, Stenevi U, Schmidt RH, Dunnett SB, Gage FH (1983) Survival and growth of nigral cell suspensions implanted in different brain sites. Acta Physiol Scand [Suppl] 522:9–18

    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

    Google Scholar 

  • Cajal SR (1929) Studies on vertebrate neurogenesis (Guth L, transi). Charles C Thomas, Springfield, 1960

    Google Scholar 

  • Candy JM, Perry RH, Perry EK, Irving D, Blessed G, Fairbairn AF, Tomlinson BE (1983) Pathological changes in the nucleus of Meynert in Alzheimer's and Parkinson's diseases. J Neurol Sci 59:277–289

    Google Scholar 

  • Dunnett SB, Low WC, Iversen SD, Stenevi U, Björklund A (1982) Septal transplants restore maze learning in rats with fornixfimbria lesions. Brain Res 251:335–348

    Google Scholar 

  • Emson PC, Koob GF (1978) The origin and distribution of dopamine-containing afferents to the rat frontal cortex. Brain Res 142:249–267

    Google Scholar 

  • Fink JS, Smith GP (1980) Mesolimbic and mesocortical dopaminergic neurons are necessary for normal exploratory behavior in rats. Neurosci Lett 17:61–65

    Google Scholar 

  • Fuxe K, Hökfelt T, Johansson O, Jonsson G, Lidbrink P, Ljungdahl A (1974) The origin of the dopamine nerve terminals in limbic and frontal cortex. Evidence for meso-cortico dopamine neurons. Brain Res 82:349–355

    Google Scholar 

  • Ghetti B, Norton J, Triarhou LC (1987) Neuroanatomical definition of the mesostriatal dopamine deficit in weaver mutant mice. Neuroscience 22:S783

    Google Scholar 

  • Herman JP, Choulli K, Geffard M, Nadaud D, Taghzouti, LeMoal M (1986) Reinnervation of the nucleus accumbens and frontal cortex of the rat by dopaminergic grafts and effects on hoarding behavior. Brain Res 372:210–216

    Google Scholar 

  • Hoh JFY (1975) Selective and non-selective reinnervation of fast-twitch and slow-twitch rat skeletal muscle. J Physiol 251:791–801

    Google Scholar 

  • Landmesser L, Pilar G (1970) Selective reinnervation of two cell populations in the adult pigeon ciliary ganglion. J Physiol 211:203–216

    Google Scholar 

  • Langley JN (1895) Note on regeneration of pre-ganglionic fibres of the sympathetic. J Physiol 18:280–284

    Google Scholar 

  • Lindvall O, Björklund A, Moore RY, Stenevi U (1974) Mesencephalic dopamine neurons projecting to neocortex. Brain Res 81:325–331

    Google Scholar 

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

    Google Scholar 

  • Pickel VM, Joh TH, Field PM, Becker CG, Reis DJ (1975) Cellular localization of tyrosine hydroxylase by immunohistochemistry. J Histochem Cytochem 23:1–12

    Google Scholar 

  • Purves D, Thompson W, Yip JW (1981) Re-innervation of ganglia transplanted to the neck from different levels of the guinea-pig sympathetic chain. J Physiol 313:49–63

    Google Scholar 

  • Routtenberg A (1978) The reward system of the brain. Sci Am 239:154–164

    Google Scholar 

  • Scarnati E, Forchetti C, Ruggieri S, Agnoli A (1980) Dopamine and dementia. An animal model with destruction of the mesocortical dopaminergic pathway: A preliminary study. In: Amaducci L, Davison AN, Antuono P (eds) Aging of the brain and dementia. Raven Press, New York, pp 139–145

    Google Scholar 

  • Scatton B, Rouquier L, Javoy-Agid F, Agid Y (1982) Dopamine deficiency in the cerebral cortex in Parkinson disease. Neurology 32:1039–1040

    Google Scholar 

  • Schmidt MJ, Sawyer BD, Perry KW, Fuller RW, Foreman MM, Ghetti B (1982) Dopamine deficiency in the weaver mutant mouse. J Neurosci 2:376–380

    Google Scholar 

  • Schultzberg M, Dunnett SB, Björklund A, Stenevi U, Hökfelt T, Dockray GJ, Goldstein M (1984) Dopamine and cholecystokinin immunoreactive neurones in mesencephalic grafts reinnervating the neostriatum: Evidence for selective growth regulation. Neuroscience 12:17–32

    Google Scholar 

  • Sharkey MA, Steedman JG, Lund RD, Dom RM (1987) Tectal transplants into the occipital cortex of the newborn rat. Dev Brain Res 31:119–123

    Google Scholar 

  • Sperry RW (1943) Effect of 180 degree rotation of the retinal field on visuomotor coordination. J Exp Zool 92:263–279

    Google Scholar 

  • Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50:703–710

    Google Scholar 

  • Sperry RW, Arora HL (1965) Selectivity in regeneration of the oculomotor nerve in the cichlid fish, Astronatus ocellatus. J Embryol Exp Morphol 14:307–317

    Google Scholar 

  • Stenevi U, Björklund A, Svendgaard N-A (1976) Transplantation of central and peripheral monoamine neurons to the adult rat brain: Techniques and conditions for survival. Brain Res 114:1–20

    Google Scholar 

  • Sternberger LA, Hardy PH, Cuculis JJ, Meyer HG (1970) The unlabeled antibody-enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-anti-horseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315–333

    Google Scholar 

  • Stone LS (1944) Functional polarization in the retinal development and its reestablishment in regenerating retinae of rotated grafted eyes. Proc Soc Exp Biol Med 57:13–14

    Google Scholar 

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

    Google Scholar 

  • Thierry AM, Tassin JP, Blanc G, Glowinski J (1976) Selective activation of the mesocortical DA system by stress. Nature (Lond) 263:242–244

    Google Scholar 

  • Triarhou LC, Low WC, Ghetti B (1986) Transplantation of ventral mesencephalic anlagen to hosts with genetic nigrostriatal dopamine deficiency. Proc Natl Acad Sci USA 83:8789–8793

    Google Scholar 

  • Triarhou LC, Low WC, Ghetti B (1987 a) Reinnervation of the dopamine deficient frontal cortex of weaver mutant mice by grafted mesencephalic dopaminergic neurones. Neuroscience 22:8257

    Google Scholar 

  • Triarhou LC, Low WC, Ghetti B (1987b) Synaptic investment of striatal cellular domains by grafted dopamine neurons in weaver mutant mice. Naturwissenschaften 74:591–593

    Google Scholar 

  • Triarhou LC, Norton J, Ghetti B (1988) Mesencephalic dopamine cell deficit involves areas A8, A9 and A10 in weaver mutant mice. Exp Brain Res 70:256–265

    Google Scholar 

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

    Google Scholar 

  • Van Essen DC, Jansen JKS (1977) The specificity of re-innervation by identified sensory and motor neurons in the leech. J Comp Neurol 171:433–454

    Google Scholar 

  • Whitehouse PJ, Hedreen JC, White CL III, Price DL (1983) Basal forebrain neurons in the dementia of Parkinson disease. Ann Neurol 13:243–248

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, Division of Neuropathology, Indiana University School of Medicine, Indianapolis, Indiana, USA

    Lazaros C. Triarhou &  Bernardino Ghetti

  2. Department of Physiology and Biophysics, Indiana University School of Medicine, Indianapolis, Indiana, USA

    Walter C. Low

  3. Program in Medical Neurobiology, Indiana University School of Medicine, Indianapolis, Indiana, USA

    Lazaros C. Triarhou, Walter C. Low &  Bernardino Ghetti

Authors
  1. Lazaros C. Triarhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Walter C. Low
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernardino Ghetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Triarhou, L.C., Low, W.C. & Ghetti, B. Layer-specific innervation of the dopamine-deficient frontal cortex in weaver mutant mice by grafted mesencephalic dopaminergic neurones. Cell Tissue Res. 254, 11–15 (1988). https://doi.org/10.1007/BF00220011

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00220011

Key words

Search

Navigation