Development of the dopaminergic innervation in the prefrontal cortex of the rat

Kalsbeek, A.; Voorn, P.; Buijs, R. M.; Pool, C. W.; Uylings, H. B. M.

doi:10.1002/cne.902690105

Cited by 545Neurotransmitter Receptor Influence on BehaviorNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

Development of the dopaminergic innervation in the prefrontal cortex of the rat

Open access

Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., Uylings, H. B. M.·1988·Journal of Comparative Neurology

DOI 10.1002/cne.902690105

Open this paper in CoChat — free account

Abstract

The pre‐ and postnatal development of the dopaminergic innervation in the prefrontal cortex (PFC) of the rat is described from embryonic day 14 through postnatal day 90. By embryonic day 15 the dopamine (DA)‐containing fibers reach the anlage of the lateral neocortex; 2 days later the first fibers have reached the subplate of the future prefrontal cortex. The process of entering the cortical plate starts just before birth. Prenatally, some dopaminergic fibers can be observed in the marginal zone of both the lateral and the medial wall of the hemisphere. Within 48 hours after birth a large number of dopaminergic fibers can be observed in the marginal zone, i.e., the future layer I, in some subareas of the PFC. A transient appearance of DA‐positive fibers is noticed in the late embryonic and early postnatal periods especially in the marginal zone and possibly in the superficial layers of the pregenual cingulate cortex. Changes in the morphology of DA fibers at P4 suggest that the actual DA innervation starts at this age. From postnatal day 6 the different subareas of the PFC can be recognized according to the characteristics of the topographical distribution of the dopaminergic fibers. Until postnatal day 60 the density of the dopaminergic fibers continues to increase. No difference in density and topography was observed between postnatal days 60 and 90.

Integrity signals

Registry

Crossref · 10.1002/cne.902690105

Cites

59 of 59 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Dopamine projections to the prefrontal cortex continue to develop into early adulthood, with dopamine levels peaking in the prefrontal cortex during adolescence versus earlier or later in life in nonhuman primates and in rats.
“Dopamine projections to the prefrontal cortex continue to develop into early adulthood, with dopamine levels peaking in the prefrontal cortex during adolescence versus earlier or later in life in nonhuman primates (Rosenberg & Lewis 1994, 1995) and in rats (Kalsbeek et al. 1988).”
From The Adolescent Brain (2008) · cites this paper as Kalsbeek et al. 1988
A subset of the medial part of the ventral tegmental area (VTA) starts to project to prefrontal subdomains around E15/E16 in rodent and week 10-13 in human.
“A subset of the medial part of the ventral tegmental area (VTA) starts to project to prefrontal subdomains around E15/E16 (rodent) and week 10–13 in human [155–158].”
From Development of prefrontal cortex (2022) · cites this paper as [158]
The unique circuitry recruited by adolescents may be associated with known structural immaturities, including continued gray matter thinning of the basal ganglia and OFC and increases in dopamine transmission.
“The unique circuitry recruited by adolescents may be associated with the known structural immaturities including continued gray matter thinning of the basal ganglia (Sowell et al., 2002) and OFC (Gogtay et al., 2004), and increases in dopamine transmission (Kalsbeek et al., 1988; Meng et al., 1999; Rosenberg & Lewis, 1994; Rosenberg & Lewis, 1995; Seeman et al., 1987).”
From Developmental changes in brain function underlying the influence of reward processing on inhibitory control (2011) · cites this paper as Kalsbeek et al., 1988
Dopamine and serotonin inputs to prefrontal cortex increase during adolescence to peak levels above earlier or later life.
“dopamine and serotonin (5-HT) inputs to PFC increase during adolescence to peak levels well above those seen earlier or later in life (Kalsbeek et al., 1988; Rosenberg and Lewis, 1994).”
From Impulsivity, frontal lobes and risk for addiction (2009) · cites this paper as Kalsbeek et al., 1988

Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals
Steinbusch, H. W. M. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90146-9 · Cited by 2,415 · see citing works
The Biochemical Basis of Neuropharmacology.
(1974) · Annals of Internal Medicine · doi:10.7326/0003-4819-81-4-575_2 · Cited by 1,882 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
Functions of the frontal cortex of the rat: A comparative review
Kolb, B. E. (1984) · Brain Research Reviews · doi:10.1016/0165-0173(84)90018-3 · Cited by 882 · see citing works
An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat
Beckstead, R. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901840104 · Cited by 792 · see citing works
Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain
Boyson, S., McGonigle, P., & Molinoff, P. B. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-11-03177.1986 · Cited by 749 · see citing works
Light‐microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny
Specht, L. A., Pickel, V. M., JOH, T. H., & Reis, D. J. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901990208 · Cited by 497 · see citing works
An immunohistochemical study of serotonin neuron development in the rat: Ascending pathways and terminal fields
Lidov, H. G. W., & Molliver, M. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90077-6 · Cited by 483 · see citing works
Organization of catecholamine neurons projecting to the frontal cortex in the rat
Lindvall, O., Björklund, A., & Divac, I. (1978) · Brain Research · doi:10.1016/0006-8993(78)90173-7 · Cited by 420 · see citing works
The serotonin innervation of the cerebral cortex in the rat—an immunohistochemical analysis
Lidov, H. G. W., Grzanna, R., & Molliver, M. E. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90099-8 · Cited by 417 · see citing works
The Biochemical Basis of Neuropharmacology
Jellinger, K. A. (2003) · European Journal of Neurology · doi:10.1046/j.1468-1331.2003.00586.x · Cited by 372 · see citing works
Brainstem innervation of prefrontal and anterior cingulate cortex in the rhesus monkey revealed by retrograde transport of HRP
Porrino, L. J., & Goldman, P. S. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902050107 · Cited by 363 · see citing works
D-1 dopamine receptors in the rat brain: a quantitative autoradiographic analysis
Dawson, T., Gehlert, D. R., McCabe, R. T., Barnett, A., & Wamsley, J. K. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-08-02352.1986 · Cited by 341 · see citing works
Biogenic amines in development
Curzon, G. (1981) · Early Human Development · doi:10.1016/0378-3782(81)90059-1 · Cited by 323 · see citing works
Cytoarchitectonic development of the prefrontal cortex in the rat
van Eden, C. G., & Uylings, H. B. M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410302 · Cited by 306 · see citing works
Self-citation
Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys
Goldman‐Rakic, P. S., & Brown, R. M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90146-8 · Cited by 283 · see citing works
Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level
van Eden, C. G., Hoorneman, E. M. D., Buijs, R. M., Matthijssen, M. A. H., Geffard, M., & Uylings, H. B. M. (1987) · Neuroscience · doi:10.1016/0306-4522(87)92964-2 · Cited by 272 · see citing works
Self-citation
Functional development of the prefrontal cortex in early life and the problem of neuronal plasticity
Goldman, P. S. (1971) · Experimental Neurology · doi:10.1016/0014-4886(71)90005-7 · Cited by 271 · see citing works
Widespread Distribution of Brain Dopamine Receptors Evidenced with [ 125 I]Iodosulpride, a Highly Selective Ligand
Martres, M., Bouthenet, M.-L., Salès, N., Sokoloff, P., & Schwartz, J.-C. (1985) · Science · doi:10.1126/science.3838821 · Cited by 267 · see citing works
First demonstration of highly specific and sensitive antibodies against dopamine
Geffard, M., Buijs, R. M., Séguéla, P., Pool, C. W., & Moal, M. L. (1984) · Brain Research · doi:10.1016/0006-8993(84)91323-4 · Cited by 250 · see citing works
Self-citation
Converging projections from the mediodorsal thalamic nucleus and mesencephalic dopaminergic neurons to the neocortex in three species
Divac, I., Björklund, A., Lindvall, O., & Passingham, R. E. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901800105 · Cited by 248 · see citing works
DEVELOPMENT OF THE UPTAKE AND STORAGE OF L‐[3H]NOREPINEPHRINE IN THE RAT BRAIN
Coyle, J. T., & Axelrod, J. L. (1971) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1971.tb05065.x · Cited by 239 · see citing works
The dopaminergic innervation of the supraoptic and paraventricular nucleus. A light and electron microscopical study
Buijs, R. M., Geffard, M., Pool, C. W., & Hoorneman, E. M. D. (1984) · Brain Research · doi:10.1016/0006-8993(84)90265-8 · Cited by 226 · see citing works
Self-citation
Development of the noradrenergic innervation of neocortex
Levitt, P., & Moore, R. Y. (1979) · Brain Research · doi:10.1016/0006-8993(79)90287-7 · Cited by 214 · see citing works
Major Innervation of Newborn Rat Cortex by Monoaminergic Neurons
Coyle, J. T., & Molliver, M. E. (1977) · Science · doi:10.1126/science.850788 · Cited by 188 · see citing works
Neurotransmitter Plasticity at the Molecular Level
Black, I. B., Adler, J. E., Dreyfus, C. F., et al. (1984) · Science · doi:10.1126/science.6147894 · Cited by 171 · see citing works
Autoregulation of fetal serotonergic neuronal development: Role of high affinity serotonin receptors
Whitaker‐Azmitia, P. M., & Azmitia, E. C. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90327-7 · Cited by 165 · see citing works
New dopaminergic terminal fields in the motor, visual (area 18b) and retrosplenial cortex in the young and adult rat. Immunocytochemical and catecholamine histochemical analyses
Berger, B., Verney, C., Alvarez, C., Vigny, A., & Helle, K. B. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90248-9 · Cited by 162 · see citing works
Transient expression of tyrosine hydroxylase immunoreactivity in some neurons of the rat neocortex during postnatal development
Berger, B., Verney, C., Gaspar, P., & Febvret, A. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90013-6 · Cited by 155 · see citing works
Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using anti-tyrosine hydroxylase antibodies
Verney, C., Berger, B., Adrien, J., Vigny, A., & Gay, M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90111-0 · Cited by 147 · see citing works
Postnatal development of serotonin nerve fibers in the somatosensory cortex of mice studied by immunohistochemistry
Fujimiya, M., Kimura, H., & Maeda, T. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460205 · Cited by 140 · see citing works
Postnatal volumetric development of the prefrontal cortex in the rat
van Eden, C. G., & Uylings, H. B. M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410303 · Cited by 135 · see citing works
Self-citation
Innervation of embryonic rat cerebral cortex by catecholamine‐containing fibers
Schlumpf, M., Shoemaker, W. J., & Bloom, F. E. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901920210 · Cited by 132 · see citing works
Regional changes in monoamines of the rat brain during postnatal development
Loizou, L. A., & Salt, P. J. (1970) · Brain Research · doi:10.1016/0006-8993(70)90177-0 · Cited by 129 · see citing works
Regional distribution of catecholamines in monkey cerebral cortex, evidence for a dopaminergic innervation of the primate prefrontal cortex
Björklund, A., Divac, I., & Lindvall, O. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90153-2 · Cited by 125 · see citing works
Catecholamines in neocortex of rhesus monkeys: regional distribution and ontogenetic development
Brown, R. M., & Goldman, P. S. (1977) · Brain Research · doi:10.1016/0006-8993(77)90960-x · Cited by 116 · see citing works
Ontogenic variations in responses to l-DOPA and monoamine receptor-stimulating agents
Kellogg, C. K., & Lundborg, P. G. (1972) · Psychopharmacology · doi:10.1007/bf00401194 · Cited by 109 · see citing works
Brain Dopamine and Serotonin Receptor Sites Revealed by Digital Subtraction Autoradiography
Altar, C. A., O’Neil, S., Walter, R. J., et al. (1985) · Science · doi:10.1126/science.2580352 · Cited by 105 · see citing works
Regional concentrations of noradrenaline and dopamine in the frontal cortex of the rat: dopaminergic innervation of the prefrontal subareas and lateralization of prefrontal dopamine
Slopsema, J. S., van der Gugten, J., & de Bruin, J. P. C. (1982) · Brain Research · doi:10.1016/0006-8993(82)90970-2 · Cited by 104 · see citing works
Distribution of norepinephrine and dopamine in cerebral cortical areas of the rat
Palkovits, M., Záborszky, L., Brownstein, M., Fekete, M. I. K., Herman, J. P., & Kanyicska, B. (1979) · Brain Research Bulletin · doi:10.1016/0361-9230(79)90099-6 · Cited by 95 · see citing works
Development of connections between the mediodorsal nucleus of the thalamus and the prefrontal cortex in the rat
van Eden, C. G. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902440307 · Cited by 89 · see citing works
Differential effects of prefrontal cortex ablation in neonatal, juvenile, and young adult rats.
Nonneman, A. J., & Corwin, J. V. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077800 · Cited by 82 · see citing works
The development of a Patchy organization of the rat striatum
Lança, A. J., Boyd, S. R., Kolb, B. E., & van der Kooy, D. (1986) · Developmental Brain Research · doi:10.1016/0165-3806(86)90226-9 · Cited by 79 · see citing works
Ontogeny of dopamine, serotonin and spirodecanone receptors in rat forebrain — An autoradiographic study
Murrin, L. C., Gibbens, D. L., & Ferrer, J. R. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90009-4 · Cited by 79 · see citing works
Axon strata of the cerebral wall in embryonic mice
Crandall, J. E., & Caviness, V. S. (1984) · Developmental Brain Research · doi:10.1016/0165-3806(84)90305-5 · Cited by 75 · see citing works
Effects of neonatal thermal lesioning of the mesocortical dopaminergic projection on the development of the rat prefrontal cortex
Kalsbeek, A., Buijs, R. M., Hofman, M. A., Matthijssen, M. A. H., Pool, C. W., & Uylings, H. B. M. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90145-3 · Cited by 72 · see citing works
Self-citation
Postnatal ontogenesis of the dopaminergic innervation in the rat anterior cingulate cortex (Area 24). Immunocytochemical and catecholamine fluorescence histochemical analysis
Berger, B., Verney, C., Febvret, A., Vigny, A., & Helle, K. B. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90021-5 · Cited by 71 · see citing works
Spontaneous and drug-induced changes of cerebral dopamine turnover during postnatal development of rats
Keller, H. H., Bartholini, G., & Pletscher, A. (1973) · Brain Research · doi:10.1016/0006-8993(73)90190-x · Cited by 54 · see citing works
Complementarity of dopaminergic and noradrenergic innervation in anterior cingulate cortex of the rat
Lewis, M. S., Molliver, M. E., Morrison, J. H., & Lidov, H. G. W. (1979) · Brain Research · doi:10.1016/0006-8993(79)90031-3 · Cited by 50 · see citing works
Prefrontal cortex: dense dopaminergic input in the newborn rat
Schmidt, R. H., Björklund, A., Lindvall, O., & Lorén, I. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90163-8 · Cited by 42 · see citing works
Dopamine‐β‐hydroxylase‐like immunoreactivity in the fetal cerebral cortex of the rat: Noradrenergic ascending pathways and terminal fields
Verney, C., Berger, B., Baulac, M., Helle, K. B., & Alvarez, C. (1984) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(84)90051-0 · Cited by 40 · see citing works
Ontogeny of open field activity in rats after neonatal lesioning of the mesocortical dopaminergic projection
Kalsbeek, A., DEBRUIN, J., Matthijssen, M. A. H., & Uylings, H. B. M. (1989) · Behavioural Brain Research · doi:10.1016/s0166-4328(89)80079-8 · Cited by 39 · see citing works
Self-citation
The catecholamine systems in the developing rat brain: improved visualization by a modified glyoxylic acid-formaldehyde method
́n, I. L., Bjo¨rklund, A., & Lindvall, O. (1976) · Brain Research · doi:10.1016/0006-8993(76)90739-3 · Cited by 34 · see citing works
Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation
Verney, C., Gaspar, P., Alvarez, C., & Berger, B. (1987) · Anatomy and Embryology · doi:10.1007/bf00310087 · Cited by 33 · see citing works
Ontogeny of (−)-[3H]norepinephrine uptake properties of synaptic storage vesicles of rat brain
Kirksey, D. F., Seidler, F. J., & Slotkin, T. A. (1978) · Brain Research · doi:10.1016/0006-8993(78)90287-1 · Cited by 26 · see citing works
Open field behavior and gross motor development in offspring of nursing rat mothers given penfluridol
Ahlenius, S., Engel, J., Hȧrd, E., et al. (1977) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(77)90034-x · Cited by 23 · see citing works
Development of specificity and stereoselectivity of rat brain dopamine receptors
Miller, J. C., & Friedhoff, A. J. (1986) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(86)90012-2 · Cited by 18 · see citing works
Extent and organization of opossum prefrontal cortex defined by anterograde and retrograde transport methods
Benjamin, R. M., & Golden, G. T. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902380107 · Cited by 12 · see citing works
Monoamine concentrations in brain regions of the developing rabbit
Crawford, I. L., Connor, J. D., & Doller, H. J. (1984) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(84)90042-x · Cited by 6 · see citing works

Flagged first, then by citations

Sorted by citations

The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The Adolescent Brain
Casey, B. J., Jones, R. M., & Hare, T. A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.010 · Cited by 3,345 · see citing works
Trajectories of brain development: point of vulnerability or window of opportunity?
Andersen, S. L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00005-8 · Cited by 1,503 · see citing works
Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082 · see citing works
Adolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines
Gillies, G. E., & McArthur, S. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002071 · Cited by 733 · see citing works
Postpubertal Emergence of Hyperresponsiveness to Stress and to Amphetamine after Neonatal Excitotoxic Hippocampal Damage: A Potential Animal Model of Schizophrenia
Lipska, B. K., Jaskiw, G. E., & Weinberger, D. R. (1993) · Neuropsychopharmacology · doi:10.1038/npp.1993.44 · Cited by 697 · see citing works
Impulsivity, frontal lobes and risk for addiction
Crews, F. T., & Boettiger, C. A. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.018 · Cited by 679 · see citing works
“For example, dopamine and serotonin (5-HT) inputs to PFC increase during adolescence to peak levels well above those seen earlier or later in life (Kalsbeek et al., 1988; Rosenberg and Lewis, 1994).”
Background
An Integrative Model of the Maturation of Cognitive Control
Luna, B., Marek, S., Larsen, B., Tervo-Clemmens, B., & Chahal, R. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034054 · Cited by 550 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
Emerging principles of altered neural circuitry in schizophrenia
Benes, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00041-7 · Cited by 513 · see citing works
Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats
Crews, F. T., Braun, C. J., Hoplight, B., Switzer, R. C., & Knapp, D. J. (2000) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2000.tb01973.x · Cited by 504 · see citing works
Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence
Cunningham, M. G., Bhattacharyya, S., & Benes, F. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10376 · Cited by 474 · see citing works
Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder.
Halperin, J. M., & Schulz, K. P. (2006) · Psychological Bulletin · doi:10.1037/0033-2909.132.4.560 · Cited by 446 · see citing works
The subplate and early cortical circuits
Kanold, P. O., & Luhmann, H. J. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153244 · Cited by 440 · see citing works
Immaturities in reward processing and its influence on inhibitory control in adolescence.
Geier, C. F., Terwilliger, R., Teslovich, T., Velanova, K., & Luna, B. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp225 · Cited by 396 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
New evidence for neurotransmitter influences on brain development
Levitt, P., Harvey, J. A., Friedman, E., Simansky, K., & Murphy, E. H. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01028-4 · Cited by 362 · see citing works
Mechanisms contributing to prefrontal cortex maturation during adolescence
Caballero, A., Granberg, R., & Tseng, K. Y. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.013 · Cited by 357 · see citing works
Development of response-monitoring ERPs in 7-to 25-year-olds
Davies, P. L., Segalowitz, S. J., & Gavin, W. J. (2004) · Developmental Neuropsychology · doi:10.1207/s15326942dn2503_6 · Cited by 339 · see citing works
Dopamine Modulation of Prefrontal Cortical Interneurons Changes during Adolescence
Tseng, K.-Y., & O'Donnell, P. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl034 · Cited by 339 · see citing works
Developmental changes in dopamine neurotransmission in adolescence: Behavioral implications and issues in assessment
Wahlstrom, D., Collins, P., White, T., & Luciana, M. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.10.013 · Cited by 311 · see citing works
“Conversely, rodents exhibit monotonic increases in dopaminergic innervation of the cortex lasting until early adulthood (Kalsbeek et al., 1988).”
Background
Transient D1Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence
Brenhouse, H. C., Sonntag, K. C., & Andersen, S. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5064-07.2008 · Cited by 287 · see citing works
Neurobehavioral evidence for changes in dopamine system activity during adolescence
Wahlstrom, D., White, T., & Luciana, M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.12.007 · Cited by 277 · see citing works
Prefrontal Cortex Development in Health and Disease: Lessons from Rodents and Humans
Chini, M., & Hanganu-Opatz, I. L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.017 · Cited by 253 · see citing works
Convergence and Plasticity of Monoaminergic Systems in the Medial Prefrontal Cortex during the Postnatal Period: Implications for the Development of Psychopathology
Benes, F. M. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1014 · Cited by 268 · see citing works
Neurogenesis in adolescent brain is potently inhibited by ethanol
Crews, F. T., Mdzinarishvili, A., Kim, D., He, J., & Nixon, K. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.090 · Cited by 265 · see citing works
Nicotine-induced conditioned place preference in adolescent and adult rats
Vastola, B. J., Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00818-1 · Cited by 251 · see citing works
Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats
Koss, W. A., Belden, C. E., Hristov, A. D., & Juraska, J. M. (2014) · Synapse · doi:10.1002/syn.21716 · Cited by 228 · see citing works
Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory
McCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
The maturation of incentive processing and cognitive control
Geier, C., & Luna, B. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.021 · Cited by 225 · see citing works
Developmental origins of brain disorders: roles for dopamine
Money, K. M., & Stanwood, G. D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00260 · Cited by 221 · see citing works
Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence
Naneix, F., Marchand, A. R., Di Scala, G., Pape, J.-R., & Coutureau, E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3080-12.2012 · Cited by 209 · see citing works
Adolescence: booze, brains, and behavior
Monti, P. M., Miranda, R., Nixon, K., Sher, K. J., Swartzwelder, H. S., Tapert, S. F., White, A., & Crews, F. T. (2005) · Alcoholism: Clinical & Experimental Research · doi:10.1097/01.alc.0000153551.11000.f3 · Cited by 206 · see citing works
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
Developmental changes in brain function underlying the influence of reward processing on inhibitory control
Padmanabhan, A., Geier, C. F., Ordaz, S. J., Teslovich, T., & Luna, B. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.004 · Cited by 202 · see citing works
Monoamine-sensitive developmental periods impacting adult emotional and cognitive behaviors
Suri, D., Teixeira, C. M., Cagliostro, M. K. C., Mahadevia, D., & Ansorge, M. S. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.231 · Cited by 167 · see citing works
Dopaminergic modulation of incentive motivation in adolescence: age-related changes in signaling, individual differences, and implications for the development of self-regulation
Luciana, M., Wahlstrom, D., Porter, J. N., & Collins, P. F. (2012) · Developmental Psychology · doi:10.1037/a0027432 · Cited by 156 · see citing works
Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus
Braun, K., Lange, E., Metzger, M., & Poeggel, G. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00420-0 · Cited by 152 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervaton of the cerebral cortex
Zecevic, N., & Verney, C. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903510404 · Cited by 149 · see citing works
Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development
Reynolds, L. M., & Flores, C. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.735625 · Cited by 137 · see citing works
The netrin receptor DCC is required in the pubertal organization of mesocortical dopamine circuitry
Manitt, C., Mimee, A., Eng, C., Pokinko, M., Stroh, T., Cooper, H. M., Kolb, B., & Flores, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0606-11.2011 · Cited by 133 · see citing works
dcc orchestrates the development of the prefrontal cortex during adolescence and is altered in psychiatric patients
Manitt, C., Eng, C., Pokinko, M., Ryan, R. T., Torres-Berrío, A., Lopez, J. P., Yogendran, S. V., Daubaras, M. J. J., Grant, A., Schmidt, E. R. E., et al. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.105 · Cited by 125 · see citing works
The emergence of gonadal hormone influences on dopaminergic function during puberty
Kuhn, C., Johnson, M., Thomae, A., Luo, B., Simon, S. A., Zhou, G., & Walker, Q. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.10.015 · Cited by 113 · see citing works
Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting
Kolk, S. M., Gunput, R.-A. F., Tran, T. S., van den Heuvel, D. M. A., Prasad, A. A., Hellemons, A. J. C. G. M., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P. H., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2521-09.2009 · Cited by 114 · see citing works
Neonatal development of projections from the basolateral amygdala to prefrontal, striatal, and thalamic structures in the rat
Bouwmeester, H., Wolterink, G., & Van Ree, J. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10084 · Cited by 112 · see citing works
The impact of junk foods on the adolescent brain
Reichelt, A. C., & Rank, M. M. (2017) · Birth Defects Research · doi:10.1002/bdr2.1173 · Cited by 102 · see citing works
The enduring effects of an adolescent social stressor on synaptic density, part II: Poststress reversal of synaptic loss in the cortex by adinazolam and MK‐801
Leussis, M. P., Lawson, K., Stone, K., & Andersen, S. L. (2008) · Synapse · doi:10.1002/syn.20483 · Cited by 95 · see citing works
Stress during a critical postnatal period induces region-specific structural abnormalities and dysfunction of the prefrontal cortex via CRF1
Yang, X.-D., Liao, X.-M., Uribe-Mariño, A., Liu, R., Xie, X.-M., Jia, J., Su, Y.-A., Li, J.-T., Schmidt, M. V., Wang, X.-D., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.304 · Cited by 93 · see citing works
Ontogeny of memory: an update on 40 years of work on infantile amnesia
Madsen, H. B., & Kim, J. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.07.030 · Cited by 92 · see citing works
The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study
Mechawar, N., & Descarries, L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00389-x · Cited by 91 · see citing works
Age and sex differences in impulsive action in rats: the role of dopamine and glutamate
Burton, C. L., & Fletcher, P. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.046 · Cited by 87 · see citing works
Ontogeny of altered dendritic morphology in the rat prefrontal cortex, hippocampus, and nucleus accumbens following Cesarean delivery and birth anoxia
Juárez, I., Gratton, A., & Flores, G. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21651 · Cited by 89 · see citing works
Development of the motivational system during adolescence, and its sensitivity to disruption by nicotine
Counotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Error-related electrocortical responses in 10-year-old children and young adults
Santesso, D. L., Segalowitz, S. J., & Schmidt, L. A. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2006.00514.x · Cited by 75 · see citing works
Early Adolescence is a Critical Period for the Maturation of Inhibitory Behavior
Reynolds, L. M., Yetnikoff, L., Pokinko, M., Wodzinski, M., Epelbaum, J. G., Lambert, L. C., Cossette, M.-P., Arvanitogiannis, A., & Flores, C. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy247 · Cited by 75 · see citing works
Early life adversity alters the developmental profiles of addiction-related prefrontal cortex circuitry
Brenhouse, H., Lukkes, J., & Andersen, S. (2013) · Brain Sciences · doi:10.3390/brainsci3010143 · Cited by 68 · see citing works
Variations in the catechol O-methyltransferase polymorphism and prefrontally guided behaviors in adolescents
Wahlstrom, D., White, T., Hooper, C. J., Vrshek-Schallhorn, S., Oetting, W. S., Brott, M. J., & Luciana, M. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.045 · Cited by 66 · see citing works
Social Defeat during Adolescence and Adulthood Differentially Induce BDNF-Regulated Immediate Early Genes
Coppens, C. M., Siripornmongcolchai, T., Wibrand, K., Alme, M. N., Buwalda, B., de Boer, S. F., Koolhaas, J. M., & Bramham, C. R. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00072 · Cited by 61 · see citing works
Dopamine-related striatal neurophysiology is associated with specialization of frontostriatal reward circuitry through adolescence
Parr, A. C., Calabro, F., Larsen, B., Tervo-Clemmens, B., Elliot, S., Foran, W., Olafsson, V., & Luna, B. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.101997 · Cited by 60 · see citing works
Prefrontal Dopaminergic Mechanisms of Extinction in Adolescence Compared to Adulthood in Rats
Zbukvic, I. C., Park, C. H. J., Ganella, D. E., Lawrence, A. J., & Kim, J. H. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00032 · Cited by 57 · see citing works
Addiction, Adolescence, and Innate Immune Gene Induction
Crews, F. T., & Vetreno, R. P. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00019 · Cited by 52 · see citing works
The effects of repeat traumatic brain injury on the pituitary in adolescent rats
Greco, T., Hovda, D., & Prins, M. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.2990 · Cited by 51 · see citing works
Adolescents let sufficient evidence accumulate before making a decision when large incentives are at stake
Teslovich, T., Mulder, M., Franklin, N. T., Ruberry, E. J., Millner, A., Somerville, L. H., Simen, P., Durston, S., & Casey, B. J. (2014) · Developmental Science · doi:10.1111/desc.12092 · Cited by 45 · see citing works
Changes in molecular composition of rat medial prefrontal cortex synapses during adolescent development
Counotte, D. S., Li, K. W., Wortel, J., Gouwenberg, Y., Van Der Schors, R. C., Smit, A. B., & Spijker, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07404.x · Cited by 47 · see citing works
Chapter 12 Age-dependent effects of lesioning the mesocortical dopamine system upon prefrontal cortex morphometry and PFC-related behaviors
Kalsbeek, A., De Bruin, J. P. C., Feenstra, M. G. P., & Uylings, H. B. M. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62684-9 · Cited by 43 · see citing works
Self-citation
Enhancing the salience of dullness: behavioral and pharmacological strategies to facilitate extinction of drug-cue associations in adolescent rats
Brenhouse, H. C., Dumais, K., & Andersen, S. L. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.063 · Cited by 38 · see citing works
Degree of neuronal activation following FG-7142 changes across regions during development
Lyss, P. J., Andersen, S. L., LeBlanc, C. J., & Teicher, M. H. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00069-3 · Cited by 37 · see citing works
Abolition of the behavioral phenotype of adult netrin-1 receptor deficient mice by exposure to amphetamine during the juvenile period
Yetnikoff, L., Almey, A., Arvanitogiannis, A., & Flores, C. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2312-6 · Cited by 30 · see citing works
Amphetamine disrupts dopamine axon growth in adolescence by a sex-specific mechanism in mice
Reynolds, L. M., Hernandez, G., MacGowan, D., Popescu, C., Nouel, D., Cuesta, S., Burke, S., Savell, K. E., Zhao, J., Restrepo-Lozano, J. M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39665-1 · Cited by 30 · see citing works
Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat
Yetnikoff, L., Reichard, R. A., Schwartz, Z. M., Parsely, K. P., & Zahm, D. S. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23459 · Cited by 30 · see citing works
Perturbed Developmental Serotonin Signaling Affects Prefrontal Catecholaminergic Innervation and Cortical Integrity
Garcia, L. P., Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1105-x · Cited by 28 · see citing works
Adolescence: a time of transition for the phenotype of dcc heterozygous mice
Yetnikoff, L., Pokinko, M., Arvanitogiannis, A., & Flores, C. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3083-z · Cited by 18 · see citing works

Embryonic mouse medial neocortex as a model system for studying the radial glial scaffold in fetal human neocortex
Vaid, S., Heikinheimo, O., & Namba, T. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02570-w · Cited by 3 · see citing works
Neocortex in early mammals and its subsequent variations
Kaas, J. H. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.05981.x · Cited by 64 · see citing works
Fez1 is layer‐specifically expressed in the adult mouse neocortex
Inoue, K., Terashima, T., Nishikawa, T., & Takumi, T. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03763.x · Cited by 59 · see citing works
Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex
Kalebic, N., Gilardi, C., Albert, M., Namba, T., Long, K. R., Kostic, M., Langen, B., & Huttner, W. Β. (2018) · eLife · doi:10.7554/elife.41241 · Cited by 129 · see citing works
Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortexPreprint
Kalebic, N., Gilardi, C., Albert, M., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/395830 · Cited by 2 · see citing works

Authors: Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., & Uylings, H. B. M.
Affiliations: Vrije Universiteit Amsterdam (NL)
ORCID: Kalsbeek, A.
Voorn, P.
Buijs, R. M.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1988-03
Volume: 269
Issue: 1
Pages: 58-72
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.902690105
OpenAlex: W2007760226
Cited by: 545
References: 59
Citations by year: 2026: 9 · 2025: 10 · 2024: 25 · 2023: 16 · 2022: 15 · 2021: 22 · 2020: 11 · 2019: 10 · 2018: 22 · 2017: 20 · 2016: 18 · 2015: 23 · 2014: 19 · 2013: 39 · 2012: 12
FWCI: 3.86
Type: journal article
Language: en
Open access: green
pure.knaw.nl
Licence: other-oa
onlinelibrary.wiley.com/termsAndConditions#vor (vor, 6066 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: dopaminergic innervation, prefrontal cortex, cortical development, embryonic development, postnatal development, subplate, marginal zone, cortical plate, topographic distribution, fiber density, rats
MeSH terms: Aging, Animals, Cerebral Cortex, Dopamine, Embryonic and Fetal Development, Frontal Lobe, Immunohistochemistry, Nerve Fibers, Rats, Inbred Strains, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Development of the dopaminergic innervation in the prefrontal cortex of the rat

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks