Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone

Tamamaki, Nobuaki; Fujimori, Kazuhiro E.; Takauji, Rumiko

doi:10.1523/jneurosci.17-21-08313.1997

Cited by 374 publications

(283 citation statements)

References 46 publications

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“…The majority of cortical interneurons are generated in the ganglionic eminence and have a long, tangential migratory pathway to arrive in the cortical plate (Anderson et al 1997;Tamamiki et al 1997). Some interneurons migrate down into the ventricular zone before migrating into the cortical plate during normal cortical development (Nadarajah et al 2002).…”

Section: Discussionmentioning

confidence: 99%

Reduction of Spontaneous Inhibitory Synaptic Activity in Experimental Heterotopic Gray Matter

Chen

Roper

2003

Journal of Neurophysiology

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Chen, Huan-Xin and Steven N. Roper. Reduction of spontaneous inhibitory synaptic activity in experimental heterotopic gray matter. J Neurophysiol 89: 150 -158, 2003. 10.1152/jn.00325.2002. Neuronal heterotopia has a strong association with epilepsy, but the mechanisms that underlie this relationship are largely unknown. We have utilized the in utero irradiated rat model to study circuit abnormalities in experimentally induced subcortical heterotopic gray matter. Spontaneous and miniature inhibitory (IPSCs) and excitatory (EPSCs) postsynaptic currents were recorded from visualized heterotopic pyramidal neurons in in vitro hemispheric slices and compared with control neocortical pyramidal neurons using the whole cell patchclamp technique. The frequency of spontaneous and miniature IPSCs was significantly reduced in pyramidal neurons from heterotopic cortex. Amplitude and kinetics of IPSCs were not different between the two groups. Spontaneous and miniature EPSCs were not different between the two groups. Short-term synaptic plasticity of stimulusevoked EPSCs showed depression in heterotopic neurons and facilitation in control pyramidal neurons. This study shows a selective impairment of the GABAergic circuitry in experimental heterotopic gray matter. We have reported similar findings in normotopic dysplastic cortex from this model. Taken together, these studies demonstrate a pervasive defect in inhibition throughout the cortex of irradiated rats with cortical dysplasia and neuronal heterotopia. This may have important implications regarding cortical development and function following in utero injuries.

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Section: Discussionmentioning

confidence: 99%

Reduction of Spontaneous Inhibitory Synaptic Activity in Experimental Heterotopic Gray Matter

Chen

Roper

2003

Journal of Neurophysiology

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“…However, cortical interneurons are generated by a distinct set of precursors located in the ventral telencephalon, more specifically in the medial and caudal parts of the ganglionic eminence [ Fig. 1A; MGE and CGE, respectively; Anderson et al, 1997;Tamamaki et al, 1997;Lavdas et al, 1999;Wichterle et al, 2001;Nery et al, 2002;Polleux et al, 2002]. At the genetic level, the generation of GABAergic cortical interneurons is under the control of distinct transcription factors: the bHLH transcription factor Mash1 and the homeodomain-containing transcription factors Dlx1 and Dlx2 [Anderson et al, 1997;Casarosa et al, 1999].…”

Section: Developmental Origin Of Gabaergic Cortical Interneuronsmentioning

confidence: 99%

Toward a developmental neurobiology of autism

Polleux

Lauder

2004

Ment. Retard. Dev. Disabil. Res. Rev.

185

132

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Autism is a complex, behaviorally defined, developmental brain disorder with an estimated prevalence of 1 in 1,000. It is now clear that autism is not a disease, but a syndrome with a strong genetic component. The etiology of autism is poorly defined both at the cellular and the molecular levels. Based on the fact that seizure activity is frequently associated with autism and that abnormal evoked potentials have been observed in autistic individuals in response to tasks that require attention, several investigators have recently proposed that autism might be caused by an imbalance between excitation and inhibition in key neural systems including the cortex. Despite considerable ongoing effort toward the identification of chromosome regions affected in autism and the characterization of many potential gene candidates, only a few genes have been reproducibly shown to display specific mutations that segregate with autism, likely because of the complex polygenic nature of this syndrome. Among those, several candidate genes have been shown to control the early patterning and/or the late synaptic maturation of specific neuronal subpopulations controlling the balance between excitation and inhibition in the developing cortex and cerebellum. In the present article, we review our current understanding of the developmental mechanisms patterning the balance between excitation and inhibition in the context of the neurobiology of autism.

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“…Unlike pyramidal neurons, which are born in the dorsal telencephalon, the majority of cortical interneurons in mice are generated in the medial ganglionic eminence (MGE) of the ventral forebrain, between embryonic day 12.5 (E12.5) and birth, and reach the cortex by tangential migration (de Carlos et al, 1996;Anderson et al, 1997;Tamamaki et al, 1997;Lavdas et al, 1999;Sussel et al, 1999;Wichterle et al, 1999;Pleasure et al, 2000;Marin and Rubenstein, 2003;Valcanis and Tan, 2003). The first population of interneurons emerging from the MGE (ϳE12.5) invade the cortex via the marginal zone (MZ), whereas subsequent waves of GABAergic interneurons populate the lower intermediate and subventricular zones (IZ/SVZ) (Corbin et al, 2001;Jimenez et al, 2002;Marin and Rubenstein, 2003;Tanaka et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Lhx6Activity Is Required for the Normal Migration and Specification of Cortical Interneuron Subtypes

Liodis¹,

Denaxa²,

Grigoriou³

et al. 2007

J. Neurosci.

363

459

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The cerebral cortex contains two main neuronal cell populations, the excitatory glutamatergic (pyramidal) neurons and the inhibitory interneurons, which synthesize GABA and constitute 20 -30% of all cortical neurons. In contrast to the mostly homogeneous population of projection neurons, cortical interneurons are characterized by remarkable morphological, molecular, and functional diversity. Among the markers that have been used to classify cortical interneurons are the calcium-binding proteins parvalbumin and calretinin and the neuropeptide somatostatin, which in rodents identify mostly nonoverlapping interneuron subpopulations. Pyramidal neurons are born during embryogenesis in the ventricular zone of the dorsal telencephalon, whereas cortical interneurons are generated in the subpallium and reach the cortex by tangential migration. On completion of tangential migration, cortical interneurons switch to a radial mode of migration and enter the cortical plate. Although the mechanisms that control the generation of interneuron diversity are currently unknown, it has been proposed that their site of origin in the ventral forebrain determines their specification into defined neurochemical subgroups. Here, we show that Lhx6, a gene induced in the medial ganglionic eminence and maintained in parvalbumin-and somatostatin-positive interneurons, is required for the specification of these neuronal subtypes in the neocortex and the hippocampus. We also show that Lhx6 activity is required for the normal tangential and radial migration of GABAergic interneurons in the cortex.

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Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone

Cited by 374 publications

References 46 publications

Reduction of Spontaneous Inhibitory Synaptic Activity in Experimental Heterotopic Gray Matter

Reduction of Spontaneous Inhibitory Synaptic Activity in Experimental Heterotopic Gray Matter

Toward a developmental neurobiology of autism

Lhx6Activity Is Required for the Normal Migration and Specification of Cortical Interneuron Subtypes

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