Regeneration, Repair, and Developmental NeuroscienceResearch PaperRegulation of early spontaneous network activity and GABAergic neurons development by thyroid hormone
Section snippets
Cell culture
Neuronal cultures were prepared from E16 rat cortex and cultured for 7 to 21 days in serum-free N2 medium. Cortical neurons were cultivated in the presence of a surrounding glial feeding layer. All experimental procedures were approved by local government authorities.
Each acid-cleaned cover slip was fitted to a 20-mm hole in the bottom of a 60-mm Petri dish, and was treated overnight with poly-D-lysine (0.1 mg/ml in borate buffer, pH 8.5, 36 °C). Astroglial cultures were prepared from cerebral
Development of spontaneous network activity
As in the neonatal cerebral cortex, synchronized rhythmic activity develops spontaneously in cortical networks formed by embryonic neurons in culture (Muramoto et al., 1993, de Lima et al., 1997, Voigt et al., 2005). The slow rhythmic synchronous Ca2+ transients seen with imaging techniques reflect bursts of action potentials recorded in single cells with the patch clamp technique (Opitz et al., 2002, Voigt et al., 2005). To illustrate the development of synchronous network activity in cultured
Hormonal modulation of network activity and synaptic maturation
Converging evidence suggests that during early neocortical development synchronous network activity emerges when neurons become interconnected. Synchronous events with very low frequency develop to reach maximal cellular participation, which includes nearly all neurons (Garaschuk et al., 2000, Opitz et al., 2002, Corlew et al., 2004). As development proceeds, synchronous events with lower cellular participation and higher burst frequency become interposed to events with higher participation,
Acknowledgments
The authors thank B. Adam and A. Ritter for expert technical assistance. This work was supported by Land Sachsen Anhalt (LSA 3431A/0302M) and Bundesministerium für Bildung und Forschung (BMBF/BNCN 016Q0702).
References (83)
- et al.
Regulation of the L1 cell adhesion molecule by thyroid hormone in the developing brain
Mol Cell Neurosci
(2000) - et al.
The developmental integration of cortical interneurons into a functional network
Curr Top Dev Biol
(2009) Developing networks play a similar melody
Trends Neurosci
(2001)- et al.
Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats
Neurosci Lett
(1996) Spontaneous correlated activity in developing neural circuits
Neuron
(1999)- et al.
Thyroid hormone regulates excitability in central neurons from postnatal rats
Neuroscience
(2004) - et al.
Early patterns of electrical activity in the developing cerebral cortex of humans and rodents
Trends Neurosci
(2006) - et al.
Thyroid hormone metabolism in primary cultures of fetal rat brain cells
Brain Res
(1985) - et al.
Role of maternal corticosterone in the development and maturation of the aminoacidergic systems of the rat brain
Int J Dev Neurosci
(2007) - et al.
Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders
Trends Neurosci
(2004)
Occipital cortico-pyramidal projection in hypothyroid rats
Brain Res Dev Brain Res
Nongenomic regulation of glutamatergic neurotransmission in hippocampus by thyroid hormones
Neuroscience
GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis
Neuron
Glutamate and GABA receptor signalling in the developing brain
Neuroscience
Frequency of synchronous oscillations of neuronal activity increases during development and is correlated to the number of synapses in cultured cortical neuron networks
Neurosci Lett
The origin of spontaneous activity in developing networks of the vertebrate nervous system
Curr Opin Neurobiol
Thyroid hormone action at the cellular, genomic and target gene levels
Mol Cell Endocrinol
Gephyrin clustering is required for the stability of GABAergic synapses
Mol Cell Neurosci
Cortical calcium waves in resting newborn mice
Nat Neurosci
Sequential generation of two distinct synapse-driven network patterns in developing neocortex
J Neurosci
Thyroid hormone regulates reelin and dab1 expression during brain development
J Neurosci
GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex
Cereb Cortex
Basic developmental rules and their implications for epilepsy in the immature brain
Epileptic Disord
GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations
Physiol Rev
Rhythms of the brain
Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones
J Physiol
Relationship between GABAergic interneurons migration and early neocortical network activity
Dev Neurobiol
Earliest spontaneous activity differentially regulates neocortical GABAergic interneuron subpopulations
Eur J Neurosci
Neuritic differentiation and synaptogenesis in neuronal cultures of the rat cerebral cortex
J Comp Neurol
Irreversible loss of a subpopulation of cortical interneurons in the absence of glutamatergic network activity
Eur J Neurosci
Identification of two distinct populations of GABAergic neurons in cultures of the rat cerebral cortex
J Comp Neurol
Astroglia inhibit the proliferation of neocortical cells and prevent the generation of small GABAergic neurons in vitro
Eur J Neurosci
Dynamics and effective topology underlying synchronization in networks of cortical neurons
J Neurosci
Dynamic nongenomic actions of thyroid hormone in the developing rat brain
Endocrinology
Identification and dynamics of spontaneous burst initiation zones in unidimensional neuronal cultures
J Neurophysiol
Large-scale oscillatory calcium waves in the immature cortex
Nat Neurosci
Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus
Endocrinology
In vivo blockade of neural activity alters dendritic development of neonatal CA1 pyramidal cells
Eur J Neurosci
Molecular organization of excitatory chemical synapses in the mammalian brain
Naturwissenschaften
Differential modulation of proliferation in the neocortical ventricular and subventricular zones
J Neurosci
Critical period regulation
Annu Rev Neurosci
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