Skip to main content
SpringerLink
Log in

Morphometric analysis of prefrontal cortical development following neonatal lesioning of the dopaminergic mesocortical projection

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

In this study the possibility that dopamine (DA) plays a trophic role in cortical development was studied by analysing cortical morphology and dendritic arborization of pyramidal cells after neonatal depletion of DA. The prefrontal cortex (PFC) was depleted of a DA innervation from postnatal day 1 onwards by thermal lesions of the DA cell group (A 10) in the ventral tegmental area. Measurements of the cortical thickness and volume of the PFC subareas did not reveal any gross alterations. The DA-depleted animals, however, showed a 30% decrease in the total length of the basal dendrites of the pyramidal cells in layer V of the medial PFC. These cells constitute the primary target of the dopaminergic innervation in the prefrontal cortex. The decreased dendritic length was due mainly to a reduced branching frequency of the basal dendrites. The present results of the dendritic measurements support a trophic role for DA in neuronal differentiation.

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

  • Bedi KS (1984) Effects of undernutrition on brain morphology: a critical review of methods and results. In: Jones DG (Ed) Current topics in research on synapses, Vol 2. Alan R Liss, New York, pp 93–163

    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

    Google Scholar 

  • Bernardi G, Cherubini E, Marciani MG, Mercuri N, Stanzione P (1982) Responses of intracellularly recorded cortical neurons to the iontophoretic application of dopamine. Brain Res 245:267–274

    Google Scholar 

  • Berry M, Bradley P, Borges S (1978) Environmental and genetic determinants of connectivity in the central nervous system: an approach trough dendritic field analysis. In: Corner MA, Baker RE, Van De Poll NE, Swaab DF, Uylings HBM (eds) Maturation of the nervous system. Progr Brain Res 48:133–149

  • Bruch L, Ebert A, Schulz E, Wenzel J (1988) Quantitativ-neuro-histologische Untersuchungen an Lamina V- und Lamina III-Pyramiden-Neuronen der Regio praecentralis agranularis der Ratte: zu Fragen der Lateralisation. J Hirnforsch 29:461–472

    Google Scholar 

  • Bunney BS, Aghajanian (1977) Electrophysiological studies of dopamine-innervated cells in the frontal cortex. In: Costa E, Gessa GL (eds) Nonstriatal dopaminergic neurons. Adv Biochem Psychopharmacol., Vol 16. Raven Press, New York, pp 47–55

    Google Scholar 

  • Buznikow GA (1984) The action of neurotransmitters and related substances on early embryogenesis. Pharmacol Ther 25:23–59

    Google Scholar 

  • Colonnier M (1964) The tangential organization of the visual cortex. J Anat Lond 98:327–344

    Google Scholar 

  • Coyle JT, Molliver ME (1977) Major innervation of newborn rat cortex by monoaminergic neurons. Science 196:444–446

    Google Scholar 

  • Doucet G, Descarries L, Audet MA, Garcia S, Berger B (1988) Radioautographic method for quantifying regional monoamine innervations in the rat brain: application to the cerebral cortex. Brain Res 441:233–259

    Google Scholar 

  • Felten DL, Hallman H, Jonsson G (1982) Evidence for a neurotrophic role of noradrenaline neurons in the postnatal development of rat cerebral cortex. J Neurocytol 11:119–135

    Google Scholar 

  • Perron A, Thierry AM, LeDouarin C, Glowinski J (1984) Inhibitory influence of the mesocortical dopaminergic system on spontaneous activity or excitatory response induced from the thalamic mediodorsal nucleus in the rat medial prefrontal cortex. Brain Res 302:257–265

    Google Scholar 

  • Friedman B, Price JL (1986) Plasticity in the olfactory cortex: age-dependent effects of deafferentation. J Comp Neurol 246:1–19

    Google Scholar 

  • Geffard M, Buijs RM, Sequela P, Pool CW, LeMoal M (1984) First demonstration of highly specific and sensitive antibodies against dopamine. Brain Res 294:161–165

    Google Scholar 

  • Hoorneman EMD (1985) Stereotaxic operation in the neoantal rat: a novel and simple procedure. J Neurosci Meth 14:109–116

    Google Scholar 

  • Iniguez C, Calle F, Marshall E, Carreres J (1987) Morphological effects of chronic haloperidol administration on the postnatal development of the striatum. Dev Brain Res 35:27–34

    Google Scholar 

  • Johnson FE, Hudd C, LaRegina MC, Beinfeld MC, Tolbert DL, Spain JW, Szucs M, Coscia CJ (1987) Exogenous cholecystokinin (CCK) reduces neonatal rat brain opioid receptor density and CCK levels. Dev Brain Res 32:139–146

    Google Scholar 

  • Kalsbeek A, Buijs RM, Hofman MA, Matthijssen MAH, Pool CW, Uylings HBM (1987) Effects of neonatal thermal lesioning of the mesocortical dopaminergic projection on the development of the rat prefrontal cortex. Dev Brain Res 32:123–132

    Google Scholar 

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

    Google Scholar 

  • Kalsbeek A, De Bruin JPC, Feenstra MGP, Matthijssen MAH, Uylings HBM (1988b) Neonatal thermal lesions of the mesolimbocortical dopaminergic projection decrease food hoarding behavior. Brain Res 475:80–90

    Google Scholar 

  • Kalsbeek A, De Bruin JPC, Matthijssen MAH, Uylings HBM (1989a) Ontogeny of open field activity in rats after neonatal lesioning of the mesocortical dopaminergic projection. Behav Brain Res 32:115–127

    Google Scholar 

  • Kalsbeek A, Feenstra MGP, Van Galen H, Uylings HBM (1989b) Monoamine and metabolite levels in the prefrontal cortex and the mesolimbic forebrain following neonatal lesions of the ventral tegmental area. Brain Res 479:339–343

    Google Scholar 

  • Kolb B, Whishaw IQ (1981) Neonatal frontal lesions in the rat: sparing of learned but not species-typical behavior in the presence of reduced brain weight and cortical thickness. J Comp Phys Psychol 95:863–879

    Google Scholar 

  • Lauder JM, Bloom FE (1974) Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. J Comp Neurol 155:469–482

    Google Scholar 

  • Lidov HG, Molliver ME (1982) The structure of cerebral cortex in the rat following prenatal administration of 6-hydroxy dopamine. Dev Brain Res 3:81–108

    Google Scholar 

  • Linden R, Pinon LGP (1987) Dual control by targets and afferents of developmental neuronal death in the mammalian central nervous system: a study in the parabigeminal nucleus of the rat. J Comp Neurol 266:141–149

    Google Scholar 

  • Lüth H-J, Werner L (1987) Morphometrische Untersuchungen im visuellen System der Ratte nach Ausschaltung noradre nerger Afferenzen mit 6-Hydroxydopamin. J Hirnforsch 28:561–569

    Google Scholar 

  • Maeda T, Tohyama M, Shimizu N (1974) Modification of postnatal development of neocortex in rat brain with experimental deprivation of locus coeruleus. Brain Res 70:515–520

    Google Scholar 

  • Mattson MP (1988) Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res Rev 13:179–212

    Google Scholar 

  • McCobb DP, Haydon PG, Kater SB (1988) Dopamine and serotonin inhibition of neurite elongation of different identified neurons. J Neurosci Res 19:19–26

    Google Scholar 

  • McMullen NT, Goldberger B, Suter CM, Glaser EM (1988) Neonatal deafening alters nonpyramidal dendrite orientation in auditory cortex: a computer microscope study in the rabbit. J Comp Neurol 267:92–106

    Google Scholar 

  • Morrison JH, Magistretti PJ (1983) Monoamines and peptides in cerbral cortex: contrasting principles of cortical organization. Trends Neurosci 4:146–151

    Google Scholar 

  • Ouimet CC, Miller PE, Hemmings HC, Walaas SI, Greengard P (1984) DARP-32, a dopamine and adenosine 3′∶5′-mo-nophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. J Neurosci 4:111–124

    Google Scholar 

  • Parnavelas JG, McDonald JK (1983) The cerebral cortex. In: Emson PC (Ed) Chemical neuroanatomy. Raven Press, New York, pp 505–549

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New York

    Google Scholar 

  • Penit-Soria J, Audinat E, Crepel F (1987) Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiological study. Brain Res 425:263–274

    Google Scholar 

  • Peterson SL, StMary JS, Harding NR (1987) Cis-Flupentixol antagonism of the rat prefrontal cortex neuronal response to apomorphine and ventral tegmental area input. Brain Res Bull 18:723–729

    Google Scholar 

  • Pinto Lord MC, Caviness VS (1979) Determinants of cell shape and orientation: a comparative Golgi analysis of cell axon interrelationships in the developing neocortex of normal and reeler mice. J Comp Neurol 187:49–70

    Google Scholar 

  • Purves D (1986) The trophic theory of neural connections. TINS 10:486–489

    Google Scholar 

  • Ramirez LF, Kalil K (1985) Critical stages for growth in the development of cortical neurons. J Comp Neurol 237:506–518

    Google Scholar 

  • Ryugo DK, Ryugo R, Killackey HP (1975a) Changes in pyra midal cell density consequent to vibrissae removal in the newborn rat. Brain Res 96:82–87

    Google Scholar 

  • Ryugo R, Ryugo DK, Killackey HP (1975b) Differential effect of enucleation on two populations of layer V pyramidal cells. Brain Res 88:554–559

    Google Scholar 

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

    Google Scholar 

  • Stewart J, Kolb B (1988) The effects of neonatal gonadectomy and prenatal stress on cortical thickness and asymmetry in rats. Behav Neural Biol 49:344–360

    Google Scholar 

  • Tennyson VM, Gershon P, Budininkas-Schoenebeck M, Rothman TP (1983) Effects of extended periods of reserpine and a-methyl-p-tyrosin treatment on the development of the putamen in fetal rabbits. Int J Dev Neurosci 1:305–318

    Google Scholar 

  • Tennyson VM, Mytilineou C, Barrett RE (1973) Fluorescence and electron microscopic studies of the early development of the substantia nigra and area ventralis tegmenti in the fetal rabbit. J Comp Neurol 149:233–258

    Google Scholar 

  • Thierry AM, LeDouarin C, Penit J, Ferron A, Glowinski J (1986) Variation in the ability of neuroleptics to block the inhibitory influence of dopaminergic neurons on the activity of cells in the rat prefrontal cortex. Brain Res Bull 16:155–160

    Google Scholar 

  • Uylings HBM, Hofman MA, Matthijssen MAH (1987) Comparison of bivariate linear relations in biological allometry research. Acta Stereol 6 (Suppl III):467–472

    Google Scholar 

  • Uylings HBM, Ruiz-Marcos A, Van Pelt J (1986a) The metric analysis of three-dimensional dendritic tree patterns: a methodological review. J Neurosci Meth 18:127–151

    Google Scholar 

  • Uylings HBM, Van Eden CG, Hofman MA (1986b) Morphometry of size/volume variables and comparison of their bivariate relations in the nervous system under different conditions. J Neurosci Meth 18:19–37

    Google Scholar 

  • Uylings HBM, Van Eden CG, Verwer RWH (1984) Morphometric methods in sexual dimorphism research on the central nervous system. In: De Vries GJ, De Bruin JPC, Uylings HBM, Corner MA (eds) Sex differences in the brain: the relation between structure and function. Progr Brain Res 61:215–222

  • Uylings HBM, Van Pelt J, Verwer RWH, McConnell P (1989) Statistical analysis of neuronal populations. In: Capowski JJ (ed) Computer techniques in neuroanatomy. Plenum Press, New York, pp 241–264

    Google Scholar 

  • Valverde F (1968) Structural changes in the area striata of the mouse after enucleation. Exp Brain Res 5:274–292

    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 microscopical level. Neuro science 22:849–862

    Google Scholar 

  • Van Eden CG, Uylings HBM (1985) Postnatal volumetric development of the prefrontal cortex in the rat. J Comp Neurol 241:268–274

    Google Scholar 

  • Wendlandt S, Crow TJ, Stirling RV (1977) The involvement of the noradrenergic system arising from the locus coeruleus in the postnatal development of the cortex in the rat brain. Brain Res 125:1–9

    Google Scholar 

  • Westrum LE, Bakay RAE (1986) Plasticity in the rat olfactory cortex. J Comp Neurol 243:195–206

    Google Scholar 

  • Zagon IS, McLaughlin PJ (1986) Opioid antagonist-induced modulation of cerebral and hippocampal development: histological and morphometric studies. Dev Brain Res 28:233–246

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Netherlands Institute for Brain Research, Meibergdreef 33, NL-1105, AZ Amsterdam, The Netherlands

    A. Kalsbeek, M. A. H. Matthijssen & H. B. M. Uylings

Authors
  1. A. Kalsbeek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. H. Matthijssen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. B. M. Uylings
    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

Kalsbeek, A., Matthijssen, M.A.H. & Uylings, H.B.M. Morphometric analysis of prefrontal cortical development following neonatal lesioning of the dopaminergic mesocortical projection. Exp Brain Res 78, 279–289 (1989). https://doi.org/10.1007/BF00228899

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00228899

Key words

Search

Navigation