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Developmental pattern changes of prefrontal efferents in the juvenile gerbil (Meriones unguiculatus)

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Summary

Previous findings of our group showed that early traumatisation leads to a dysfunctional organisation of prefrontocortical efferents in adulthood. To identify vulnerable time windows during maturation, we labelled either layer III- or layer V/VI-pyramidal cells with biocytin in the prefrontal cortex of gerbils (Meriones unguiculatus) from the age of postnatal day (PD) 15 up to adulthood (PD 90). The density of passing fibres and axonal terminals in distinct cortical columns in specific prefrontal projection areas was assessed by digital image analysis. Following layer III injections, fibre densities reached adult values between adolescence (PD 60) and adulthood (PD 90). However, layer V/VI-fibre densities decreased after eye-opening (PD 15), followed by an increase to adult values after weaning (PD 30). These findings are the first to describe dynamic structural changes even beyond adolescence of functionally diverse prefrontal output systems. External interventions might exert adverse influences on the establishment of integrated prefrontal networks especially during the early phase of re-arranging.

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References

  • SA Anderson JD Classey F Conde JS Lund DA Lewis (1995) ArticleTitleSynchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex Neuroscience 67 7–22 Occurrence Handle7477911 Occurrence Handle10.1016/0306-4522(95)00051-J Occurrence Handle1:CAS:528:DyaK2MXmtFOitrg%3D

    Article  PubMed  CAS  Google Scholar 

  • F Bagorda G Teuchert-Noodt K Lehmann (2006) ArticleTitleIsolation rearing or methamphetamine traumatisation induce a “dysconnection” of prefrontal efferents in gerbils: implications for schizophrenia J Neural Transm 113 365–379 Occurrence Handle15959840 Occurrence Handle10.1007/s00702-005-0324-2 Occurrence Handle1:STN:280:DC%2BD28%2Fmsl2hsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • MC Ballesteros PE Hansen K Soila (1993) ArticleTitleMR imaging of the developing human brain. Part 2. Postnatal development Radiographics 13 611–622 Occurrence Handle8316668 Occurrence Handle1:STN:280:DyaK3szgtlehtg%3D%3D

    PubMed  CAS  Google Scholar 

  • AP Bannister (2005) ArticleTitleInter- and intra-laminar connections of pyramidal cells in the neocortex Neurosci Res 53 95–103 Occurrence Handle16054257 Occurrence Handle10.1016/j.neures.2005.06.019

    Article  PubMed  Google Scholar 

  • A Batardiere P Barone K Knoblauch P Giroud M Berland AM Dumas H Kennedy (2002) ArticleTitleEarly specification of the hierarchical organization of visual cortical areas in the macaque monkey Cereb Cortex 12 453–465 Occurrence Handle11950763 Occurrence Handle10.1093/cercor/12.5.453

    Article  PubMed  Google Scholar 

  • B Berger C Verney A Febvret A Vigny KB Helle (1985) ArticleTitlePostnatal ontogenesis of the dopaminergic innervation in the rat anterior cingulate cortex (area 24). Immunocytochemical and catecholamine fluorescence histochemical analysis Brain Res 353 31–47 Occurrence Handle2862963 Occurrence Handle1:STN:280:DyaL2M3otFGgsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • J Berger-Sweeney CF Hohmann (1997) ArticleTitleBehavioral consequences of abnormal cortical development: insights into developmental disabilities Behav Brain Res 86 121–142 Occurrence Handle9134147 Occurrence Handle10.1016/S0166-4328(96)02251-6 Occurrence Handle1:STN:280:DyaK2s3nvFOnsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JP Bourgeois PS Goldman-Rakic P Rakic (1994) ArticleTitleSynaptogenesis in the prefrontal cortex of rhesus monkeys Cereb Cortex 4 78–96 Occurrence Handle8180493 Occurrence Handle10.1093/cercor/4.1.78 Occurrence Handle1:STN:280:DyaK2c3jsF2kuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • BA Brody HC Kinney AS Kloman FH Gilles (1987) ArticleTitleSequence of central nervous system myelination in human infancy. I. An autopsy study of myelination J Neuropathol Exp Neurol 46 283–301 Occurrence Handle3559630 Occurrence Handle1:STN:280:DyaL2s7mvVGgtA%3D%3D

    PubMed  CAS  Google Scholar 

  • VJ Brown EM Bowman (2002) ArticleTitleRodent models of prefrontal cortical function Trends Neurosci 25 340–343 Occurrence Handle12079756 Occurrence Handle10.1016/S0166-2236(02)02164-1 Occurrence Handle1:CAS:528:DC%2BD38XksFKrsb8%3D

    Article  PubMed  CAS  Google Scholar 

  • Brummelte S, Witte AV, Teuchert-Noodt G (2007) Postnatal development of GABA and Calbindin cells and fibers in the prefrontal cortex and basolateral amygdala of gerbils (Meriones unguiculatus). Int J Dev Neurosci [Epub ahead of print]

  • A Busche D Polascheck J Lesting J Neddens G Teuchert-Noodt (2004) ArticleTitleDevelopmentally induced imbalance of dopaminergic fibre densities in limbic brain regions of gerbils (Meriones unguiculatus) J Neural Transm 111 451–463 Occurrence Handle15057515 Occurrence Handle10.1007/s00702-004-0106-2 Occurrence Handle1:STN:280:DC%2BD2c7mtlOnsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • B Clancy RB Darlington BL Finlay (2001) ArticleTitleTranslating developmental time across mammalian species Neuroscience 105 7–17 Occurrence Handle11483296 Occurrence Handle10.1016/S0306-4522(01)00171-3 Occurrence Handle1:CAS:528:DC%2BD3MXlsFymt7s%3D

    Article  PubMed  CAS  Google Scholar 

  • I Coman G Barbin P Charles B Zalc C Lubetzki (2005) ArticleTitleAxonal signals in central nervous system myelination, demyelination and remyelination J Neurol Sci 233 67–71 Occurrence Handle15894333 Occurrence Handle10.1016/j.jns.2005.03.029 Occurrence Handle1:CAS:528:DC%2BD2MXltVeju7g%3D

    Article  PubMed  CAS  Google Scholar 

  • JW Dalley RN Cardinal TW Robbins (2004) ArticleTitlePrefrontal executive and cognitive functions in rodents: neural and neurochemical substrates Neurosci Biobehav Rev 28 771–784 Occurrence Handle15555683 Occurrence Handle10.1016/j.neubiorev.2004.09.006 Occurrence Handle1:CAS:528:DC%2BD2cXhtVSlurnJ

    Article  PubMed  CAS  Google Scholar 

  • RR Dawirs G Teuchert-Noodt R Czaniera (1993a) ArticleTitleMaturation of the dopamine innervation during postnatal development of the prefrontal cortex in gerbils (Meriones unguiculatus). A quantitative immunocytochemical study J Hirnforsch 34 281–290 Occurrence Handle1:STN:280:DyaK2c%2FpsFyhuw%3D%3D

    CAS  Google Scholar 

  • RR Dawirs G Teuchert-Noodt M Molthagen (1993b) ArticleTitleIndication of methamphetamine-induced reactive synaptogenesis in the prefrontal cortex of gerbils (Meriones unguiculatus) Eur J Pharmacol 241 89–97 Occurrence Handle10.1016/0014-2999(93)90937-D Occurrence Handle1:CAS:528:DyaK2cXktFw%3D

    Article  CAS  Google Scholar 

  • RR Dawirs G Teuchert-Noodt R Czaniera (1994) ArticleTitleThe postnatal maturation of dopamine innervation in the prefrontal cortex of gerbils (Meriones unguiculatus) is sensitive to an early single dose of methamphetamine. A quantitative immunocytochemical study J Hirnforsch 35 195–204 Occurrence Handle8064138 Occurrence Handle1:STN:280:DyaK2czkt1Ohuw%3D%3D

    PubMed  CAS  Google Scholar 

  • VB De Graaf-Peters M Hadders-Algra (2006) ArticleTitleOntogeny of the human central nervous system: what is happening when? Early Hum Dev 82 257–266 Occurrence Handle16360292 Occurrence Handle10.1016/j.earlhumdev.2005.10.013

    Article  PubMed  Google Scholar 

  • C Dehay J Bullier H Kennedy (1984) ArticleTitleTransient projections from the fronto-parietal and temporal cortex to areas 17, 18 and 19 in the kitten Exp Brain Res 57 208–212 Occurrence Handle6519228 Occurrence Handle10.1007/BF00231149 Occurrence Handle1:STN:280:DyaL2M7gtFyjuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J Dodd TM Jessell (1988) ArticleTitleAxon guidance and the patterning of neuronal projections in vertebrates Science 242 692–699 Occurrence Handle3055291 Occurrence Handle10.1126/science.3055291 Occurrence Handle1:CAS:528:DyaL1MXjs12lsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D Eilam (1997) ArticleTitlePostnatal development of body architecture and gait in several rodent species J Exp Biol 200 1339–1350 Occurrence Handle9172418 Occurrence Handle1:STN:280:DyaK2szhs1GjtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • I Feinberg (1982) ArticleTitleSchizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17 319–334 Occurrence Handle7187776 Occurrence Handle10.1016/0022-3956(82)90038-3

    Article  PubMed  Google Scholar 

  • RD Frostig (2006) ArticleTitleFunctional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box Curr Opin Neurobiol 16 445–450 Occurrence Handle16822663 Occurrence Handle10.1016/j.conb.2006.06.001 Occurrence Handle1:CAS:528:DC%2BD28Xns1Grtr0%3D

    Article  PubMed  CAS  Google Scholar 

  • JM Fuster (2002) ArticleTitleFrontal lobe and cognitive development J Neurocytol 31 373–385 Occurrence Handle12815254 Occurrence Handle10.1023/A:1024190429920

    Article  PubMed  Google Scholar 

  • PL Gabbott TA Warner PR Jays SJ Bacon (2003) ArticleTitleAreal and synaptic interconnectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat Brain Res 993 59–71 Occurrence Handle14642831 Occurrence Handle10.1016/j.brainres.2003.08.056 Occurrence Handle1:CAS:528:DC%2BD3sXpt1elt7g%3D

    Article  PubMed  CAS  Google Scholar 

  • JN Giedd J Blumenthal NO Jeffries FX Castellanos H Liu A Zijdenbos T Paus AC Evans JL Rapoport (1999) ArticleTitleBrain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 2 861–863 Occurrence Handle10491603 Occurrence Handle10.1038/13158 Occurrence Handle1:CAS:528:DyaK1MXmsVOqu7s%3D

    Article  PubMed  CAS  Google Scholar 

  • PS Goldman-Rakic (1987) ArticleTitleDevelopment of cortical circuitry and cognitive function Child Dev 58 601–622 Occurrence Handle3608641 Occurrence Handle10.2307/1130201 Occurrence Handle1:STN:280:DyaL2s3nsFWksA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • PJ Harrison (1999) ArticleTitleThe neuropathology of schizophrenia. A critical review of the data and their interpretation Brain 122 IssueIDPt 4 593–624 Occurrence Handle10219775 Occurrence Handle10.1093/brain/122.4.593

    Article  PubMed  Google Scholar 

  • PW Hickmott M Constantine-Paton (1997) ArticleTitleExperimental down-regulation of the NMDA channel associated with synapse pruning J Neurophysiol 78 1096–1107 Occurrence Handle9307137 Occurrence Handle1:CAS:528:DyaK2sXls1Onsrs%3D

    PubMed  CAS  Google Scholar 

  • F Hu SM Strittmatter (2004) ArticleTitleRegulating axon growth within the postnatal central nervous system Semin Perinatol 28 371–378 Occurrence Handle15693393 Occurrence Handle10.1053/j.semperi.2004.10.001

    Article  PubMed  Google Scholar 

  • PR Huttenlocher (1979) ArticleTitleSynaptic density in human frontal cortex – developmental changes and effects of aging Brain Res 163 195–205 Occurrence Handle427544 Occurrence Handle10.1016/0006-8993(79)90349-4 Occurrence Handle1:STN:280:DyaE1M7ks1eitg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • PR Huttenlocher AS Dabholkar (1997) ArticleTitleRegional differences in synaptogenesis in human cerebral cortex J Comp Neurol 387 167–178 Occurrence Handle9336221 Occurrence Handle10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z Occurrence Handle1:STN:280:DyaK2svnsF2ksg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • PR Huttenlocher de Court (1987) ArticleTitleThe development of synapses in striate cortex of man Hum Neurobiol 6 1–9 Occurrence Handle3583840 Occurrence Handle1:STN:280:DyaL2s3itFOqsg%3D%3D

    PubMed  CAS  Google Scholar 

  • GM Innocenti (1981) ArticleTitleGrowth and reshaping of axons in the establishment of visual callosal connections Science 212 824–827 Occurrence Handle7221566 Occurrence Handle10.1126/science.7221566 Occurrence Handle1:STN:280:DyaL3M7nslSkuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • GM Innocenti DJ Price (2005) ArticleTitleExuberance in the development of cortical networks Nat Rev Neurosci 6 955–965 Occurrence Handle16288299 Occurrence Handle10.1038/nrn1790 Occurrence Handle1:CAS:528:DC%2BD2MXht12ntbvL

    Article  PubMed  CAS  Google Scholar 

  • GO Ivy HJ Gould SuffixIII HP Killackey (1984) ArticleTitleVariability in the distribution of callosal projection neurons in the adult rat parietal cortex Brain Res 306 53–61 Occurrence Handle6205722 Occurrence Handle10.1016/0006-8993(84)90355-X Occurrence Handle1:STN:280:DyaL2c3otFOltg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • GO Ivy HP Killackey (1981) ArticleTitleThe ontogeny of the distribution of callosal projection neurons in the rat parietal cortex J Comp Neurol 195 367–389 Occurrence Handle6162864 Occurrence Handle10.1002/cne.901950302 Occurrence Handle1:STN:280:DyaL3M7kt1yhsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • KM Jacobs JP Donoghue (1991) ArticleTitleReshaping the cortical motor map by unmasking latent intracortical connections Science 251 944–947 Occurrence Handle2000496 Occurrence Handle10.1126/science.2000496 Occurrence Handle1:STN:280:DyaK3M7lslSisw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G Jeffery BJ Arzymanow AR Lieberman (1984) ArticleTitleDoes the early exuberant retinal projection to the superior colliculus in the neonatal rat develop synaptic connections? Brain Res 316 135–138 Occurrence Handle6733532 Occurrence Handle1:STN:280:DyaL2c3jtlCnuw%3D%3D

    PubMed  CAS  Google Scholar 

  • TL Jernigan SL Archibald MT Berhow ER Sowell DS Foster JR Hesselink (1991) ArticleTitleCerebral structure on MRI, Part I: localization of age-related changes Biol Psychiatry 29 55–67 Occurrence Handle2001446 Occurrence Handle10.1016/0006-3223(91)90210-D Occurrence Handle1:STN:280:DyaK3M7lvFGquw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • EG Jones (1984) Laminar distribution of cortical efferent cells A Peters EG Jones (Eds) Cerebral cortex Plenum Press New York 521–553

    Google Scholar 

  • A Kalsbeek RM Buijs MA Hofman MA Matthijssen CW Pool HB Uylings (1987) ArticleTitleEffects of neonatal thermal lesioning of the mesocortical dopaminergic projection on the development of the rat prefrontal cortex Brain Res 429 123–132 Occurrence Handle3032369 Occurrence Handle1:STN:280:DyaL2s7os1Glsw%3D%3D

    PubMed  CAS  Google Scholar 

  • A Kalsbeek P Voorn RM Buijs CW Pool HB Uylings (1988) ArticleTitleDevelopment of the dopaminergic innervation in the prefrontal cortex of the rat J Comp Neurol 269 58–72 Occurrence Handle3361004 Occurrence Handle10.1002/cne.902690105 Occurrence Handle1:STN:280:DyaL1c7pvVKqsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • LC Katz CJ Shatz (1996) ArticleTitleSynaptic activity and the construction of cortical circuits Science 274 1133–1138 Occurrence Handle8895456 Occurrence Handle10.1126/science.274.5290.1133 Occurrence Handle1:CAS:528:DyaK28XmvVOru7w%3D

    Article  PubMed  CAS  Google Scholar 

  • H Kennedy J Bullier C Dehay (1989) ArticleTitleTransient projection from the superior temporal sulcus to area 17 in the newborn macaque monkey Proc Natl Acad Sci USA 86 8093–8097 Occurrence Handle2479015 Occurrence Handle10.1073/pnas.86.20.8093 Occurrence Handle1:STN:280:DyaK3c%2Fks1Ontg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • MS Keshavan GE Hogarty (1999) ArticleTitleBrain maturational processes and delayed onset in schizophrenia Dev Psychopathol 11 525–543 Occurrence Handle10532623 Occurrence Handle10.1017/S0954579499002199 Occurrence Handle1:STN:280:DC%2BD3c%2FgtVChsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • HP Killackey LM Chalupa (1986) ArticleTitleOntogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey J Comp Neurol 244 331–348 Occurrence Handle3958231 Occurrence Handle10.1002/cne.902440306 Occurrence Handle1:STN:280:DyaL287mvFSjtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JH Kim JM Juraska (1997) ArticleTitleSex differences in the development of axon number in the splenium of the rat corpus callosum from postnatal day 15 through 60 Brain Res Dev Brain Res 102 77–85 Occurrence Handle9298236 Occurrence Handle10.1016/S0165-3806(97)00080-1 Occurrence Handle1:CAS:528:DyaK2sXksFehsr0%3D

    Article  PubMed  CAS  Google Scholar 

  • MA Kingsbury ER Graf BL Finlay (2000) ArticleTitleAltered development of visual subcortical projections following neonatal thalamic ablation in the hamster J Comp Neurol 424 165–178 Occurrence Handle10888746 Occurrence Handle10.1002/1096-9861(20000814)424:1<165::AID-CNE12>3.0.CO;2-U Occurrence Handle1:STN:280:DC%2BD3cvitFWqtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • MA Kingsbury NA Lettman BL Finlay (2002) ArticleTitleReduction of early thalamic input alters adult corticocortical connectivity Brain Res Dev Brain Res 138 35–43 Occurrence Handle12234656 Occurrence Handle10.1016/S0165-3806(02)00456-X Occurrence Handle1:CAS:528:DC%2BD38XntVeitL0%3D

    Article  PubMed  CAS  Google Scholar 

  • B Kolb (1984) ArticleTitleFunctions of the frontal cortex of the rat: a comparative review Brain Res 320 65–98 Occurrence Handle6440660 Occurrence Handle1:STN:280:DyaL2M%2FpvVKlsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • R Lent C Hedin-Pereira JR Menezes S Jhaveri (1990) ArticleTitleNeurogenesis and development of callosal and intracortical connections in the hamster Neuroscience 38 21–37 Occurrence Handle2175019 Occurrence Handle10.1016/0306-4522(90)90371-A Occurrence Handle1:STN:280:DyaK3M%2FnsVenuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • P Levitt (2003) ArticleTitleStructural and functional maturation of the developing primate brain J Pediatr 143 S35–S45 Occurrence Handle14597912 Occurrence Handle10.1067/S0022-3476(03)00400-1 Occurrence Handle1:CAS:528:DC%2BD3sXpsFyks7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • HG Lidov ME Molliver (1982) ArticleTitleAn immunohistochemical study of serotonin neuron development in the rat: ascending pathways and terminal fields Brain Res Bull 8 389–430 Occurrence Handle6178481 Occurrence Handle10.1016/0361-9230(82)90077-6 Occurrence Handle1:STN:280:DyaL383jtlSltA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • LK Low HJ Cheng (2006) ArticleTitleAxon pruning: an essential step underlying the developmental plasticity of neuronal connections Philos Trans R Soc Lond B Biol Sci 361 1531–1544 Occurrence Handle16939973 Occurrence Handle10.1098/rstb.2006.1883 Occurrence Handle1:CAS:528:DC%2BD28XhtFakurfE

    Article  PubMed  CAS  Google Scholar 

  • H Markram J Lubke M Frotscher A Roth B Sakmann (1997) ArticleTitlePhysiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex J Physiol 500 IssueIDPt 2 409–440 Occurrence Handle9147328 Occurrence Handle1:CAS:528:DyaK2sXjtVWqsr8%3D

    PubMed  CAS  Google Scholar 

  • DS Melchitzky SR Sesack ML Pucak DA Lewis (1998) ArticleTitleSynaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex J Comp Neurol 390 211–224 Occurrence Handle9453665 Occurrence Handle10.1002/(SICI)1096-9861(19980112)390:2<211::AID-CNE4>3.0.CO;2-4 Occurrence Handle1:STN:280:DyaK1c7hsVCisg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • BD Mitchell JD Macklis (2005) ArticleTitleLarge-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice J Comp Neurol 482 17–32 Occurrence Handle15612019 Occurrence Handle10.1002/cne.20428

    Article  PubMed  Google Scholar 

  • F Murakami WJ Song H Katsumaru (1992) ArticleTitlePlasticity of neuronal connections in developing brains of mammals Neurosci Res 15 235–253 Occurrence Handle1337578 Occurrence Handle10.1016/0168-0102(92)90045-E Occurrence Handle1:STN:280:DyaK3s7msFaitA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J Neddens F Bagorda A Busche S Horstmann GH Moll RR Dawirs G Teuchert-Noodt (2003) ArticleTitleEpigenetic factors differentially influence postnatal maturation of serotonin (5-HT) innervation in cerebral cortex of gerbils: interaction of rearing conditions and early methamphetamine challenge Brain Res Dev Brain Res 146 119–130 Occurrence Handle14643018 Occurrence Handle10.1016/j.devbrainres.2003.09.016 Occurrence Handle1:CAS:528:DC%2BD3sXpt1eksbg%3D

    Article  PubMed  CAS  Google Scholar 

  • J Neddens RR Dawirs F Bagorda A Busche S Horstmann G Teuchert-Noodt (2004) ArticleTitlePostnatal maturation of cortical serotonin lateral asymmetry in gerbils is vulnerable to both environmental and pharmacological epigenetic challenges Brain Res 1021 200–208 Occurrence Handle15342268 Occurrence Handle10.1016/j.brainres.2004.06.050 Occurrence Handle1:CAS:528:DC%2BD2cXntlSntbs%3D

    Article  PubMed  CAS  Google Scholar 

  • M Nossoll G Teuchert-Noodt RR Dawirs (1997) ArticleTitleA single dose of methamphetamine in neonatal gerbils affects adult prefrontal gamma-aminobutyric acid innervation Eur J Pharmacol 340 R3–R5 Occurrence Handle9537803 Occurrence Handle1:CAS:528:DyaK2sXotVyjs7o%3D

    PubMed  CAS  Google Scholar 

  • JL Nunez DM Lauschke JM Juraska (2001) ArticleTitleCell death in the development of the posterior cortex in male and female rats J Comp Neurol 436 32–41 Occurrence Handle11413544 Occurrence Handle10.1002/cne.1051 Occurrence Handle1:STN:280:DC%2BD3MzkvFOksA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J Olavarria RC Van Sluyters (1985) ArticleTitleOrganization and postnatal development of callosal connections in the visual cortex of the rat J Comp Neurol 239 1–26 Occurrence Handle4044927 Occurrence Handle10.1002/cne.902390102 Occurrence Handle1:STN:280:DyaL28%2FgvFSrsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JG Parnavelas HB Uylings (1980) ArticleTitleThe growth of non-pyramidal neurons in the visual cortex of the rat: a morphometric study Brain Res 193 373–382 Occurrence Handle7388598 Occurrence Handle10.1016/0006-8993(80)90171-7 Occurrence Handle1:STN:280:DyaL3c3it1Wiug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G Paxinos C Watson (2005) The rat brain in stereotaxic coordinates EditionNumber5 Academic Press New York

    Google Scholar 

  • A Pfefferbaum DH Mathalon EV Sullivan JM Rawles RB Zipursky KO Lim (1994) ArticleTitleA quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood Arch Neurol 51 874–887 Occurrence Handle8080387 Occurrence Handle1:STN:280:DyaK2czmtFKhuw%3D%3D

    PubMed  CAS  Google Scholar 

  • DJ Price C Blakemore (1985) ArticleTitleRegressive events in the postnatal development of association projections in the visual cortex Nature 316 721–724 Occurrence Handle3839903 Occurrence Handle10.1038/316721a0 Occurrence Handle1:STN:280:DyaL2M3ps1ejsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DJ Price H Kennedy C Dehay L Zhou M Mercier Y Jossin AM Goffinet F Tissir D Blakey Z Molnar (2006) ArticleTitleThe development of cortical connections Eur J Neurosci 23 910–920 Occurrence Handle16519656 Occurrence Handle10.1111/j.1460-9568.2006.04620.x

    Article  PubMed  Google Scholar 

  • JM Provis DD van FA Billson P Russell (1985) ArticleTitleHuman fetal optic nerve: overproduction and elimination of retinal axons during development J Comp Neurol 238 92–100 Occurrence Handle4044906 Occurrence Handle10.1002/cne.902380108 Occurrence Handle1:STN:280:DyaL28%2FgvFSmsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • MV Puig F Artigas P Celada (2005) ArticleTitleModulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: involvement of serotonin and GABA Cereb Cortex 15 1–14 Occurrence Handle15238448 Occurrence Handle10.1093/cercor/bhh104

    Article  PubMed  Google Scholar 

  • S Rathjen R Engelmann S Struif T Kaulisch D Stiller S Lowel (2003) ArticleTitleThe growth of cat cerebral cortex in postnatal life: a magnetic resonance imaging study Eur J Neurosci 18 1797–1806 Occurrence Handle14622214 Occurrence Handle10.1046/j.1460-9568.2003.02909.x

    Article  PubMed  Google Scholar 

  • D Rice SJ Barone (2000) ArticleTitleCritical periods of vulnerability for the developing nervous system: evidence from humans and animal models Environ Health Perspect 108 IssueIDSuppl 3 511–533 Occurrence Handle10852851 Occurrence Handle10.2307/3454543

    Article  PubMed  Google Scholar 

  • D Riddle A Richards F Zsuppan D Purves (1992) ArticleTitleGrowth of the rat somatic sensory cortex and its constituent parts during postnatal development J Neurosci 12 3509–3524 Occurrence Handle1527593 Occurrence Handle1:STN:280:DyaK38vgslKhtA%3D%3D

    PubMed  CAS  Google Scholar 

  • JE Rose CN Woolsey (1984) ArticleTitleThe orbitofrontal cortex and its connections with the mediodorsal nucleus in rabbit, sheep and cat Res Publ Assoc Nerv Ment Dis 27 210–232

    Google Scholar 

  • JK Seamans N Gorelova D Durstewitz CR Yang (2001) ArticleTitleBidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons J Neurosci 21 3628–3638 Occurrence Handle11331392 Occurrence Handle1:CAS:528:DC%2BD3MXjs1antb8%3D

    PubMed  CAS  Google Scholar 

  • SR Sesack AY Deutch RH Roth BS Bunney (1989) ArticleTitleTopographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J Comp Neurol 290 213–242 Occurrence Handle2592611 Occurrence Handle10.1002/cne.902900205 Occurrence Handle1:STN:280:DyaK3c%2FnvVOntg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DL Sherman PJ Brophy (2005) ArticleTitleMechanisms of axon ensheathment and myelin growth Nat Rev Neurosci 6 683–690 Occurrence Handle16136172 Occurrence Handle10.1038/nrn1743 Occurrence Handle1:CAS:528:DC%2BD2MXpslaksr8%3D

    Article  PubMed  CAS  Google Scholar 

  • MS Sodhi E Sanders-Bush (2004) ArticleTitleSerotonin and brain development Int Rev Neurobiol 59 111–174 Occurrence Handle15006487 Occurrence Handle1:CAS:528:DC%2BD2cXktVert7c%3D Occurrence Handle10.1016/S0074-7742(04)59006-2

    Article  PubMed  CAS  Google Scholar 

  • ER Sowell DA Trauner A Gamst TL Jernigan (2002) ArticleTitleDevelopment of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study Dev Med Child Neurol 44 4–16 Occurrence Handle11811649 Occurrence Handle10.1017/S0012162201001591

    Article  PubMed  Google Scholar 

  • NC Spitzer (1991) ArticleTitleA developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation J Neurobiol 22 659–673 Occurrence Handle1722506 Occurrence Handle10.1002/neu.480220702 Occurrence Handle1:STN:280:DyaK387htlGqtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • G Tamas EH Buhl A Lorincz P Somogyi (2000) ArticleTitleProximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons Nat Neurosci 3 366–371 Occurrence Handle10725926 Occurrence Handle10.1038/73936 Occurrence Handle1:CAS:528:DC%2BD3cXitlagtrk%3D

    Article  PubMed  CAS  Google Scholar 

  • M Tessier-Lavigne CS Goodman (1996) ArticleTitleThe molecular biology of axon guidance Science 274 1123–1133 Occurrence Handle8895455 Occurrence Handle10.1126/science.274.5290.1123 Occurrence Handle1:CAS:528:DyaK28XmvVOrtbc%3D

    Article  PubMed  CAS  Google Scholar 

  • G Teuchert-Noodt RR Dawirs (1991) ArticleTitleAge-related toxicity in prefrontal cortex and caudate-putamen complex of gerbils (Meriones unguiculatus) after a single dose of methamphetamine Neuropharmacology 30 733–743 Occurrence Handle1922686 Occurrence Handle10.1016/0028-3908(91)90181-A Occurrence Handle1:CAS:528:DyaK3MXlt1KqsLk%3D

    Article  PubMed  CAS  Google Scholar 

  • AM Thomson AP Bannister (1998) ArticleTitlePostsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex Neuroscience 84 669–683 Occurrence Handle9579775 Occurrence Handle10.1016/S0306-4522(97)00557-5 Occurrence Handle1:CAS:528:DyaK1cXitVOiurg%3D

    Article  PubMed  CAS  Google Scholar 

  • KY Tseng P O’Donnell (2004) ArticleTitleDopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms J Neurosci 24 5131–5139 Occurrence Handle15175382 Occurrence Handle10.1523/JNEUROSCI.1021-04.2004 Occurrence Handle1:CAS:528:DC%2BD2cXkvFOktrs%3D

    Article  PubMed  CAS  Google Scholar 

  • HB Uylings CG van Eden (1990) ArticleTitleQualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans Prog Brain Res 85 31–62 Occurrence Handle2094901 Occurrence Handle1:STN:280:DyaK3M3ks1Ohsw%3D%3D Occurrence Handle10.1016/S0079-6123(08)62675-8

    Article  PubMed  CAS  Google Scholar 

  • CG Van Eden JM Kros HB Uylings (1990) ArticleTitleThe development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas Prog Brain Res 85 169–183 Occurrence Handle2094893 Occurrence Handle1:STN:280:DyaK3M3ks1OisQ%3D%3D

    PubMed  CAS  Google Scholar 

  • CG Van Eden HB Uylings (1985) ArticleTitlePostnatal volumetric development of the prefrontal cortex in the rat J Comp Neurol 241 268–274 Occurrence Handle4086657 Occurrence Handle10.1002/cne.902410303 Occurrence Handle1:STN:280:DyaL287ht1KitQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JR Villablanca TD Schmanke V Lekht HA Crutcher (2000) ArticleTitleThe growth of the feline brain from late fetal into adult life. I. A morphometric study of the neocortex and white matter Brain Res Dev Brain Res 122 11–20 Occurrence Handle10915901 Occurrence Handle10.1016/S0165-3806(00)00046-8 Occurrence Handle1:CAS:528:DC%2BD3cXltVOmt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • PD Wall TJ Coderre Y Stern Z Wiesenfeld-Hallin (1988) ArticleTitleSlow changes in the flexion reflex of the rat following arthritis or tenotomy Brain Res 447 215–222 Occurrence Handle3390692 Occurrence Handle10.1016/0006-8993(88)91122-5 Occurrence Handle1:STN:280:DyaL1c3ntVSguw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • DR Weinberger BK Lipska (1995) ArticleTitleCortical maldevelopment, anti-psychotic drugs, and schizophrenia: a search for common ground Schizophr Res 16 87–110 Occurrence Handle7577773 Occurrence Handle10.1016/0920-9964(95)00013-C Occurrence Handle1:STN:280:DyaK28%2FhtVCksQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • KT Winterfeld G Teuchert-Noodt RR Dawirs (1998) ArticleTitleSocial environment alters both ontogeny of dopamine innervation of the medial prefrontal cortex and maturation of working memory in gerbils (Meriones unguiculatus) J Neurosci Res 52 201–209 Occurrence Handle9579410 Occurrence Handle10.1002/(SICI)1097-4547(19980415)52:2<201::AID-JNR8>3.0.CO;2-E Occurrence Handle1:CAS:528:DyaK1cXisFeltro%3D

    Article  PubMed  CAS  Google Scholar 

  • AV Witte F Bagorda G Teuchert-Noodt K Lehmann (2007) ArticleTitleContralateral prefrontal projections in gerbils mature abnormally after early methamphetamine trauma and isolated rearing J Neural Transm 114 285–288 Occurrence Handle16715206 Occurrence Handle10.1007/s00702-006-0506-6 Occurrence Handle1:STN:280:DC%2BD2s%2Fjs1Srsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • TU Woo AL Crowell (2005) ArticleTitleTargeting synapses and myelin in the prevention of schizophrenia Schizophr Res 73 193–207 Occurrence Handle15653262 Occurrence Handle10.1016/j.schres.2004.07.022

    Article  PubMed  Google Scholar 

  • PI Yakovlev (1962) ArticleTitleMorphological criteria of growth and maturation of the nervous system in man Res Publ Assoc Res Nerv Ment Dis 39 3–46 Occurrence Handle14008721 Occurrence Handle1:STN:280:DyaF383gtVKgtA%3D%3D

    PubMed  CAS  Google Scholar 

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  1. Department of Neuroanatomy, Faculty of Biology, University of Bielefeld, Bielefeld, Germany

    A. V. Witte, S. Brummelte & G. Teuchert-Noodt

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  1. A. V. Witte
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  2. S. Brummelte
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  3. G. Teuchert-Noodt
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Witte, A., Brummelte, S. & Teuchert-Noodt, G. Developmental pattern changes of prefrontal efferents in the juvenile gerbil (Meriones unguiculatus). J Neural Transm 114, 1377–1393 (2007). https://doi.org/10.1007/s00702-007-0761-1

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