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Sequential generation of two distinct synapse-driven network patterns in developing neocortex
- Source :
- Journal of Neuroscience, Journal of Neuroscience, Society for Neuroscience, 2008, 28 (48), pp.12851-63. ⟨10.1523/JNEUROSCI.3733-08.2008⟩
- Publication Year :
- 2008
- Publisher :
- HAL CCSD, 2008.
-
Abstract
- International audience; Developing cortical networks generate a variety of coherent activity patterns that participate in circuit refinement. Early network oscillations (ENOs) are the dominant network pattern in the rodent neocortex for a short period after birth. These large-scale calcium waves were shown to be largely driven by glutamatergic synapses albeit GABA is a major excitatory neurotransmitter in the cortex at such early stages, mediating synapse-driven giant depolarizing potentials (GDPs) in the hippocampus. Using functional multineuron calcium imaging together with single-cell and field potential recordings to clarify distinct network dynamics in rat cortical slices, we now report that the developing somatosensory cortex generates first ENOs then GDPs, both patterns coexisting for a restricted time period. These patterns markedly differ by their developmental profile, dynamics, and mechanisms: ENOs are generated before cortical GDPs (cGDPs) by the activation of glutamatergic synapses mostly through NMDARs; cENOs are low-frequency oscillations (approximately 0.01 Hz) displaying slow kinetics and gradually involving the entire network. At the end of the first postnatal week, GABA-driven cortical GDPs can be reliably monitored; cGDPs are recurrent oscillations (approximately 0.1 Hz) that repetitively synchronize localized neuronal assemblies. Contrary to cGDPs, cENOs were unexpectedly facilitated by short anoxic conditions suggesting a contribution of glutamate accumulation to their generation. In keeping with this, alterations of extracellular glutamate levels significantly affected cENOs, which are blocked by an enzymatic glutamate scavenger. Moreover, we show that a tonic glutamate current contributes to the neuronal membrane excitability when cENOs dominate network patterns. Therefore, cENOs and cGDPs are two separate aspects of neocortical network maturation that may be differentially engaged in physiological and pathological processes.
- Subjects :
- MESH: Synaptic Potentials
MESH: gamma-Aminobutyric Acid
Somatosensory system
Synaptic Transmission
MESH: Animals, Newborn
Membrane Potentials
MESH: Synapses
Synapse
0302 clinical medicine
MESH: Animals
MESH: Hypoxia, Brain
Cortical Synchronization
Hypoxia, Brain
gamma-Aminobutyric Acid
0303 health sciences
Neocortex
General Neuroscience
Glutamate receptor
Articles
MESH: Glutamic Acid
Synaptic Potentials
medicine.anatomical_structure
MESH: Rats
Neurogenesis
MESH: Biological Clocks
Glutamic Acid
[SDV.BC]Life Sciences [q-bio]/Cellular Biology
Biology
MESH: Calcium Signaling
Receptors, N-Methyl-D-Aspartate
MESH: Somatosensory Cortex
03 medical and health sciences
Glutamatergic
Calcium imaging
Organ Culture Techniques
Giant depolarizing potentials
Biological Clocks
medicine
MESH: Synaptic Transmission
Animals
MESH: Cortical Synchronization
MESH: Membrane Potentials
Calcium Signaling
Rats, Wistar
[SDV.BC] Life Sciences [q-bio]/Cellular Biology
030304 developmental biology
MESH: Receptors, N-Methyl-D-Aspartate
Extracellular Fluid
Somatosensory Cortex
MESH: Rats, Wistar
MESH: Organ Culture Techniques
Rats
MESH: Neurogenesis
Animals, Newborn
MESH: Extracellular Fluid
MESH: Nerve Net
Synapses
Nerve Net
Neuroscience
030217 neurology & neurosurgery
Subjects
Details
- Language :
- English
- ISSN :
- 02706474 and 15292401
- Database :
- OpenAIRE
- Journal :
- Journal of Neuroscience, Journal of Neuroscience, Society for Neuroscience, 2008, 28 (48), pp.12851-63. ⟨10.1523/JNEUROSCI.3733-08.2008⟩
- Accession number :
- edsair.doi.dedup.....76a41dac0c4b220c8b9b5b8bfdbcf420