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Spontaneous electrical activity in the human fetal cortex in vitro.

ABSTRACT: Our knowledge about the developing human cerebral cortex is based on the analysis of fixed postmortem material. Here we use electrical recordings from unfixed human postmortem tissue to characterize the synaptic physiology and spontaneous network activity of pioneer cortical neurons ("subplate neurons"). Our electrophysiological experiments show that functional glutamate or GABA ionotropic receptors are expressed on human subplate (SP) neurons as early as 20 gestational weeks. Extracellular (synaptic) stimulations evoked postsynaptic potentials in a very small fraction of SP neurons, suggesting that functional synaptic contacts are rare at midgestation. Although synaptic inputs were scarce, we regularly observed spontaneous (unprovoked) electrical activity among human SP neurons, comprised of sustained plateau depolarizations and bursts of action potential firing, which resembled cortical UP and DOWN states in the adult neocortex. Plateau depolarizations and bursts of action potential firing are thought to depend on the mature morphology and physiology of adult cortical network. However, our current data reveal that similar cortical rhythm is generated by a very immature ensemble of human fetal neurons. In the relative absence of sensory inputs, as in development in utero, or in slow-wave sleep (i.e., throughout the entire lifespan), the spontaneous slow oscillatory pattern (UP and DOWN states) is a fundamental aspect of human cortical physiology.

SUBMITTER: Moore AR

PROVIDER: S-EPMC3564513 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Spontaneous electrical activity in the human fetal cortex in vitro.

Moore Anna R AR Zhou Wen-Liang WL Jakovcevski Igor I Zecevic Nada N Antic Srdjan D SD

The Journal of neuroscience : the official journal of the Society for Neuroscience 20110201 7

Our knowledge about the developing human cerebral cortex is based on the analysis of fixed postmortem material. Here we use electrical recordings from unfixed human postmortem tissue to characterize the synaptic physiology and spontaneous network activity of pioneer cortical neurons ("subplate neurons"). Our electrophysiological experiments show that functional glutamate or GABA ionotropic receptors are expressed on human subplate (SP) neurons as early as 20 gestational weeks. Extracellular (syn ...[more]

PMID: 21325506

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Project description:IntroductionCa2+ release from sarcoplasmic reticulum (SR) is known to contribute to automaticity via the cytoplasmic Na+-Ca2+ exchanger (NCX). Mitochondria participate in Ca2+ cycling. We studied the role of mitochondrial Ca2+ flux in ventricular spontaneous electrical activity.MethodsSpontaneously contracting mouse embryonic stem cells (ESC)-derived ventricular cardiomyocytes (CMs) were differentiated from wild type and ryanodine receptor type 2 (RYR2) knockout mouse ESCs and differentiated for 19-21 days. Automaticity was also observed in human induced pluripotent stem cell (hiPSC)-derived ventricular CMs differentiated for 30 days, and acute isolated adult mouse ventricular cells in ischemic simulated buffer. Action potentials (APs) were recorded by perforated whole cell current-clamp. Cytoplasmic and mitochondrial Ca2+ transients were determined by fluorescent imaging.ResultsIn mouse ESC-derived ventricular CMs, spontaneous beating was dependent on the L-type Ca2+ channel, cytoplasmic NCX and mitochondrial NCX. Spontaneous beating was modulated by SR Ca2+ release from RYR2 or inositol trisphosphate receptors (IP3R), the pacemaker current (If) and mitochondrial Ca2+ uptake by the mitochondrial Ca2+ uniporter (MCU). In RYR2 knockout mouse ESC-derived ventricular CMs, mitochondrial Ca2+ flux influenced spontaneous beating independently of the SR Ca2+ release from RYR2, and the mitochondrial effect was dependent on IP3R SR Ca2+ release. Depolarization of mitochondria and preservation of ATP could terminate spontaneous beating. A contribution of mitochondrial Ca2+ flux to automaticity was confirmed in hiPSC-derived ventricular CMs and ischemic adult mouse ventricular CMs, confirming the findings across species and cell maturity levels.ConclusionsMitochondrial and sarcolemma NCX fluxes are required for ventricular automaticity. Mitochondrial Ca2+ uptake plays a modulatory role. Mitochondrial Ca2+ uptake through MCU is influenced by IP3R-dependent SR Ca2+ release.

Project description:The medial frontal cortex remains functionally ill-understood; this is reflected by the heterogeneity of behavioural outcomes following damage to the region. We aim to use the rich information provided by extraoperative direct electrical cortical stimulation to enhance our understanding of its functional anatomy. Examining a cohort of 38 epilepsy patients undergoing direct electrical cortical stimulation in the context of presurgical evaluation, we reviewed stimulation findings and classified them in a behavioural framework (positive motor, negative motor, somatosensory, speech disturbances, and "other"). The spatially discrete cortical stimulation-derived data points were then transformed into continuous probabilistic maps, thereby enabling the voxel-wise spatial inference widely used in the analysis of functional and structural imaging data. A functional map of stimulation findings of the medial wall emerged. Positive motor responses occurred in 141 stimulations (31.2%), anatomically located on the paracentral lobule (threshold at p<.05), extending no further than the vertical anterior commissure (VCA) line. Thirty negative motor responses were observed (6.6%), localised to the VCA line (at p < .001 uncorrected). In 43 stimulations (9.5%) a somatosensory response localised to the caudal cingulate zone (at p < .001 uncorrected), with a second region posterior to central sulcus. Speech disturbances were elicited in 38 stimulations (8.4%), more commonly but not exclusively from the language fMRI dominant side, just anterior to VCA (p < .001 uncorrected). In only 2 stimulations, the patient experienced a subjective "urge" to move in the absence of overt movement. Classifying motor behaviour along the dimensions of effector, and movement vs arrest, we derive a wholly data-driven stimulation map of the medial wall, powered by the largest number of stimulations of the region reported (n = 452) in patients imaged with MRI. This model and the underlying data provide a robust framework for understanding the architecture of the region through the joint analysis of disruptive and correlative anatomical maps.

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Spontaneous electrical activity in the human fetal cortex in vitro.

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Spontaneous electrical activity in the human fetal cortex in vitro.

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