Clusters of Coupled Neuroblasts in Embryonic Neocortex

Turco, JJ Lo; Kriegstein, AR

doi:10.1126/science.1850552

Cited by 313 publications

(203 citation statements)

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“…Na ؉ Channel Stimulation in PP Cells Triggers Glutamate Secretion. At E13, synapses have not been formed yet (22), and gap junctions are not present in differentiated neuronal cells (8,23), suggesting that Ca 2ϩ increases in cells devoid of Na ϩ channels probably involve extracellular signaling. GABA and glutamate are good candidates because (i) they are present in the mouse neocortex as early as E10 (4), (ii) they both lead to a Ca 2ϩ increase (5), and (iii) they are known to be involved in early corticogenesis (24).…”

Section: Resultsmentioning

confidence: 99%

“…This observation suggests that there might be an additional and indirect mechanism involved in the spreading of the response. At this early stage of neurogenesis, synapses have not yet formed (22), and gap junctions are not present in differentiated neuronal cells (8,23). Radial glial cells could take part in communication between PP and VZ cells as it was demonstrated later in development (31).…”

Section: Discussionmentioning

confidence: 99%

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Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate

Platel

Boisseau

Dupuis

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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Before synaptogenesis, early excitability implicating voltagedependent and transmitter-activated channels is known to be crucial for neuronal development. We previously showed that preplate (PP) neurons of the mouse neocortex express functional Na ؉ channels as early as embryonic day 12. In this study, we investigated the role of these Na ؉ channels in signaling during early development. In the neocortex of embryonic-day-13 mice, activation of Na ؉ channels with veratridine induced a large Ca 2؉ response throughout the neocortex, even in cell populations that lack the Na ؉ channel. This Na ؉ -dependent Ca 2؉ activity requires external Ca 2؉ and is completely blocked by inhibitors of Na ؉ ͞Ca 2؉ exchangers. Moreover, veratridine-induced Ca 2؉ increase coincides with a burst of exocytosis in the PP. In parallel, we show that Na ؉ channel stimulation enhances glutamate secretion in the neocortical wall. Released glutamate triggers further Ca 2؉ response in PP and ventricular zone, as indicated by the decreased response to veratridine in the presence of ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor and NMDA-receptor inhibitors. Therefore, the combined activation of the Na ؉ channel and the Na ؉ ͞Ca 2؉ exchanger triggers Ca 2؉ signaling in the PP neurons, leading to glutamate secretion, which amplifies the signal and serves as an autocrine͞paracrine transmitter before functional synapses are formed in the neocortex. Membrane depolarization induced by glycine receptors activation could be one physiological activator of this Na ؉ channel-dependent pathway.Ca 2ϩ signaling ͉ Na ϩ ͞Ca 2ϩ exchanger ͉ exocytosis ͉ neurogenesis N eurons in the cerebral cortex are generated in a proliferative region known as the ventricular zone (VZ) (1). The first phase of neurogenesis occurs at embryonic days 11-13 (E11-E13) in mice and gives rise to a group of neurons that form the preplate (PP) above the VZ (2).During development, ligand-and voltage-gated ionic currents appear in a complex and progressive pattern, generating cell excitability. This early excitability has a widespread and important role in transmission of information and development of the nervous system. Combinations of ion channels usually generate Ca 2ϩ influx, which influences differentiation and regulates channel expression (for review, see ref.3). Neurotransmitters are reported to be present very early during neurogenesis (4). GABA and glutamate are both present in the neocortical wall and can regulate neuronal progenitor proliferation (4, 5) and neuronal migration (6). Taurine and glycine are also present and have been reported to be the most abundant neurotransmitters at E13 in mouse neocortex (7). Little is known about the channels and pathways that are involved in this early activity, and particularly little is known about how these neurotransmitters are secreted before the appearance of voltage-dependent Ca 2ϩ channels (8,9).Although cells are devoid of synaptic connection, spontaneous Ca 2ϩ activity is already present at E13 (J.-C.P. and M.A., u...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate

Platel

Boisseau

Dupuis

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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“…Intracellular acidification also blocks gap junctions (Turin and Warner, 1980;Lo Turco and Kriegstein, 1991). Low-pH TEA Krebs (pH 6.8) produced a reversible depolarization of 10 -20 mV accompanied by a decreased frequency of spontaneous synchronous activity (n ϭ 10) (Fig.…”

Section: Gap Junction Blockers Disrupt Oscillationsmentioning

confidence: 99%

“…Control of the population of LC cells was obtained only with the superfusion of agents that affected many cells, such as AMPA and ME. Finally, two manipulations known to block electrotonic coupling in other sites, carbenoxolone and low pH, reduced or abolished the synchronous oscillations in membrane potential (Turin and Warner, 1980;Davidson et al, 1986;Davidson and Baumgarten, 1988;Lo Turco and Kriegstein, 1991;Martin et al, 1991). Taken together, the results suggest that electrotonic coupling between adult neurons may account for the synchronous activity.…”

Section: Synchronous Activitymentioning

confidence: 99%

Synchronous Activity in Locus Coeruleus Results from Dendritic Interactions in Pericoerulear Regions

1996

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Locus coeruleus (LC) neurons in brain slices from adult rats were studied using intracellular and extracellular recordings to investigate synchronous activity. Spontaneous field potentials were recorded with extracellular electrodes in solutions containing tetraethylammonium chloride (10 mM) and BaCl 2 (1 mM). These field potentials were found throughout but not outside the LC cell body region. No field potentials were observed in control solutions. Paired recordings showed that field potentials were synchronous in all areas of the LC. The synchronous activity was resistant to tetrodotoxin (1 M) and to the neurotransmitter receptor blockers D-2-amino-5-phosphonopentanoic acid, bicuculline, 6-cyano-7-nitroquinoxaline-2,3-dione, idazoxan, and strychnine, suggesting that this activity was not synaptically driven. Field potentials were also synchronous with oscillations in membrane potential recorded with intracellular electrodes. The oscillations in membrane potential were 5-30 mV in amplitude and had a biphasic waveform. Neither the frequency nor the waveform of the oscillations was dependent on the membrane potential. The glycyrrhetinic acid derivative carbenoxolone and intracellular acidification with CO 2 disrupted synchronous activity, suggesting a role of electrotonic coupling. When the cell body region of the LC was isolated from the pericoerulear dendritic regions by sectioning the slice rostral and caudal to the cell body region, synchronous activity was reduced or abolished. Dendritic interaction in the pericoerulear region was also indicated by improved voltage control of the opioid-induced potassium current, as indicated by a shift in the reversal potential to the potassium equilibrium potential. The results suggest that electrical interactions between dendrites outside the cell body region can account for synchronous activity within the nucleus.

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“…Thus, communication through gap junctions is an important requirement for the maintenance of normal nuclear movement in retinal progenitor cells (Pearson et al 2005). Progenitors in the VZ are also connected by gap junctions (LoTurco and Kriegstein 1991;Bittman et al 1997); therefore, it is likely that similar regulatory mechanisms involving gap junctions and calcium transients are functional there as well (Elias and Kriegstein 2008).…”

Section: Cell Polarity and Interkinetic Nuclear Movementsmentioning

confidence: 99%

Interkinetic Nuclear Movement in the Ventricular Zone of the Cortex

2011

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The nuclei of neuroepithelial cells move along the apicobasal axis in synchronization with their cell cycle status. This motility is known as interkinetic nuclear movement. We discuss here the importance of cytoskeleton organization, the centrosome, molecular motors, cell polarity proteins, and their regulators in controlling and maintaining this typical behavior. Furthermore, due to the tight linkage between cell proliferation, cell cycle, and nuclear motility, we speculate that interkinetic nuclear movement is likely to be affected in the pathophysiology of microcephaly, where the brain size is markedly reduced.

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Clusters of Coupled Neuroblasts in Embryonic Neocortex

Cited by 313 publications

References 33 publications

Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate

Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate

Synchronous Activity in Locus Coeruleus Results from Dendritic Interactions in Pericoerulear Regions

Interkinetic Nuclear Movement in the Ventricular Zone of the Cortex

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Clusters of Coupled Neuroblasts in Embryonic Neocortex

Cited by 313 publications

References 33 publications

Na + channel-mediated Ca 2+ entry leads to glutamate secretion in mouse neocortical preplate

Na + channel-mediated Ca 2+ entry leads to glutamate secretion in mouse neocortical preplate

Synchronous Activity in Locus Coeruleus Results from Dendritic Interactions in Pericoerulear Regions

Interkinetic Nuclear Movement in the Ventricular Zone of the Cortex

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Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate

Na ⁺ channel-mediated Ca ²⁺ entry leads to glutamate secretion in mouse neocortical preplate