Regulation of Laminar and Area Patterning of Mammalian Neocortex and Behavioural Implications

O’Leary, Dennis D.M.; Chou, Shen Ju; Hamasaki, Tadashi; Sahara, Setsuko; Takeuchi, Atsushi; Thuret, Sandrine; Leingärtner, Axel

doi:10.1002/9780470994030.ch11

Cited by 13 publications

(19 citation statements)

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“…The four pallial regions characteristic of the telencephalon of tetrapods have been identified in Pleurodeles by their distinct staining patterns of several neuronal markers and transcription factors (Moreno and Gonz alez, 2007a;Morona and Gonz alez, 2008;Joven et al, 2013). Thus, we referred to medial, dorsal, lateral, and ventral pallial regions in the description of the distribution of Pax6 expression, the only Pax gene that has been demonstrated to have multiple roles during the formation of the pallium/cortex (Yun et al, 2001;Bachy et al, 2002;Bishop et al, 2002;Jim enez et al, 2002;Muzio et al, 2002;Schuurmans and Guillemot, 2002;Assimacopoulos et al, 2003;Talamillo et al, 2003;Carney et al, 2006;O'Leary et al, 2007;Quinn et al, 2007;Tamai et al, 2007;Gopal and Golden, 2008;Piñon et al, 2008;Tuoc et al, 2009;Ceci et al, 2010;Cocas et al, 2011;Georgala et al, 2011). In Pleurodeles, like in other tetrapods (Smith-Fern andez et al, 1998;Puelles et al, 2000), Pax6 is a general marker of the pallial neuroepithelium during the embryonic period.…”

Section: Palliummentioning

confidence: 99%

Spatiotemporal Patterns of Pax3, Pax6, and Pax7 Expression in the Developing Brain of a Urodele Amphibian, Pleurodeles waltl

Joven

Morona

González

et al. 2013

J of Comparative Neurology

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The onset and developmental dynamics of Pax3, Pax6, and Pax7 expressions were analyzed by immunohistochemical techniques in the central nervous system (CNS) of embryos, larvae, and recently metamorphosed juveniles of the urodele amphibian Pleurodeles waltl. During the embryonic period, the Pax proteins start being detectable in neuroepithelial domains. Subsequently, they become restricted to subsets of cells in distinct brain regions, maintaining different degrees of expression in late larvae and juvenile brains. Specifically, Pax6 is broadly expressed all along the urodele CNS (olfactory bulbs, pallium, basal ganglia, diencephalon, mesencephalic tegmentum, rhombencephalon, and spinal cord) and the developing olfactory organ and retina. Pax3 and Pax7 are excluded from the rostral forebrain and were usually observed in overlapping regions during embryonic development, whereas Pax3 expression is highly downregulated as development proceeds. Thus, Pax3 is restricted to the roof plate of prosomere 2, pretectum, optic tectum, rhombencephalon, and spinal cord. Comparatively, Pax7 was more conspicuous in all these regions. Pax7 cells were also found in the paraphysis, intermediate lobe of the hypophysis, and basal plate of prosomere 3. Our data show that the expression patterns of the three Pax genes studied are overall evolutionarily conserved, and therefore could unequivocally be used to identify subdivisions in the urodele brain similar to other vertebrates, which are not clearly discernable with classical techniques. In addition, the spatiotemporal sequences of expression provide indirect evidence of putative migratory routes across neuromeric limits and the alar-basal boundary.

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Section: Palliummentioning

confidence: 99%

Spatiotemporal Patterns of Pax3, Pax6, and Pax7 Expression in the Developing Brain of a Urodele Amphibian, Pleurodeles waltl

Joven

Morona

González

et al. 2013

J of Comparative Neurology

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“…Even though there is evidence that thalamic projections to the cortex play roles in cortical areal differentiation (Sur et al, 1990; O'Leary et al, 1994, 2007), the basic aspects of this thalamic morphogenetic role are not well-understood. The initial basic specification of cortical areas seems to be determined by intrinsic cortical factors, without direct thalamic influence (Rakic, 1988).…”

Section: Introductionmentioning

confidence: 99%

Growth of Thalamocortical Fibers to the Somatosensory Cortex in the Human Fetal Brain

et al. 2017

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Thalamocortical (TH-C) fiber growth begins during the embryonic period and is completed by the third trimester of gestation in humans. Here we determined the timing and trajectories of somatosensory TH-C fibers in the developing human brain. We analyzed the periods of TH-C fiber outgrowth, path-finding, “waiting” in the subplate (SP), target selection, and ingrowth in the cortical plate (CP) using histological sections from post-mortem fetal brain [from 7 to 34 postconceptional weeks (PCW)] that were processed with acetylcholinesterase (AChE) histochemistry and immunohistochemical methods. Images were compared with post mortem diffusion tensor imaging (DTI)-based fiber tractography (code No NO1-HD-4-3368). The results showed TH-C axon outgrowth occurs as early as 7.5 PCW in the ventrolateral part of the thalamic anlage. Between 8 and 9.5 PCW, TH-C axons form massive bundles that traverse the diencephalic-telencephalic boundary. From 9.5 to 11 PCW, thalamocortical axons pass the periventricular area at the pallial-subpallial boundary and enter intermediate zone in radiating fashion. Between 12 and 14 PCW, the TH-C axons, aligned along the fibers from the basal forebrain, continue to grow for a short distance within the deep intermediate zone and enter the deep CP, parallel with SP expansion. Between 14 and 18 PCW, the TH-C interdigitate with callosal fibers, running shortly in the sagittal stratum and spreading through the deep SP (“waiting” phase). From 19 to 22 PCW, TH-C axons accumulate in the superficial SP below the somatosensory cortical area; this occurs 2 weeks earlier than in the frontal and occipital cortices. Between 23 and 24 PCW, AChE-reactive TH-C axons penetrate the CP concomitantly with its initial lamination. Between 25 and 34 PCW, AChE reactivity of the CP exhibits an uneven pattern suggestive of vertical banding, showing a basic 6-layer pattern. In conclusion, human thalamocortical axons show prolonged growth (4 months), and somatosensory fibers precede the ingrowth of fibers destined for frontal and occipital areas. The major features of growing TH-C somatosensory fiber trajectories are fan-like radiation, short runs in the sagittal strata, and interdigitation with the callosal system. These results support our hypothesis that TH-C axons are early factors in SP and CP morphogenesis and synaptogenesis and may regulate cortical somatosensory system maturation.

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“…The complex structure of the human neocortex underlies increased behavioral and cognitive capacity that allows for enhanced sensory perception, motor control, spatial reasoning, and conscious thoughts (Bystron et al, 2008; Guillery, 2005; Markram et al, 2004; O'Leary et al, 2007). The neocortex is composed of six layers with functionally distinct subdivisions, which contain diverse neuronal populations that make both local and extrinsic connections (O'Leary et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…The neocortex is composed of six layers with functionally distinct subdivisions, which contain diverse neuronal populations that make both local and extrinsic connections (O'Leary et al, 2007). These layers originate from a homogenous pseudo-stratified epithelium that lines the lateral ventricle in the dorsal telencephalon.…”

Section: Introductionmentioning

confidence: 99%

“…These layers originate from a homogenous pseudo-stratified epithelium that lines the lateral ventricle in the dorsal telencephalon. Through a coordinated sequence of proliferation and migration, the layers form in an ‘inside-out sequence’ with the last migrating cells arriving at the most superficial portion of layer II by postnatal day (PD) 6 (Ignacio et al, 1995; O'Leary et al, 2007; Parnavelas, 2000). In rodents, cortical GABAergic interneurons arise from pseudo-stratified epithelia that lines the medial ganglionic eminence (Anderson et al, 2001; Parnavelas, 2000).…”

Section: Introductionmentioning

confidence: 99%

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Modulation of GABAergic and glutamatergic transmission by ethanol in the developing neocortex: An in vitro test of the excessive inhibition hypothesis of fetal alcohol spectrum disorder

2009

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SummaryExposure to ethanol during development triggers neuronal cell death and this is thought to play a central role in the pathophysiology of fetal alcohol spectrum disorder (FASD). Studies suggest that ethanol-induced neurodegeneration during the period of synaptogenesis results from widespread potentiation of GABA A receptors and inhibition of NMDA receptors throughout the brain, with neocortical layer II being particularly sensitive. Here, we tested whether ethanol modulates the function of these receptors during this developmental period using patch-clamp electrophysiological and Ca 2+ imaging techniques in acute slices from postnatal day 7-9 rats. We focused on pyramidal neurons in layer II of the parietal cortex (with layer III as a control). Ethanol (70 mM) increased spontaneous action potential-dependent GABA release in layer II (but not layer III) neurons without affecting postsynaptic GABA A receptors. Protein and mRNA expression for both the Cl − importer, NKCC1, and the Cl − exporter KCC2, were detected in layer II/III neurons. Perforated-patch experiments demonstrated that E Cl − is shifted to the right of E m ; activation of GABA A receptors with muscimol depolarized E m , decreased action potential firing, and minimally increased [Ca 2+ ] i . However, the ethanol-induced increase of GABAergic transmission did not affect neuronal excitability. Ethanol had no effect on currents exogenously evoked by NMDA or AMPA receptor-mediated spontaneous excitatory postsynaptic currents. Acute application of ethanol in the absence of receptor antagonists minimally increased [Ca 2+ ] i . These findings are inconsistent with the excessive inhibition model of ethanol-induced neurodegeneration, supporting the view that ethanol damages developing neurons via more complex mechanisms that vary among specific neuronal populations.

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Regulation of Laminar and Area Patterning of Mammalian Neocortex and Behavioural Implications

Cited by 13 publications

References 0 publications

Spatiotemporal Patterns of Pax3, Pax6, and Pax7 Expression in the Developing Brain of a Urodele Amphibian, Pleurodeles waltl

Spatiotemporal Patterns of Pax3, Pax6, and Pax7 Expression in the Developing Brain of a Urodele Amphibian, Pleurodeles waltl

Growth of Thalamocortical Fibers to the Somatosensory Cortex in the Human Fetal Brain

Modulation of GABAergic and glutamatergic transmission by ethanol in the developing neocortex: An in vitro test of the excessive inhibition hypothesis of fetal alcohol spectrum disorder

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