Sequential generation of two distinct synapse-driven network patterns in developing neocortex.
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.
Allène
Camille
C
Institut de Neurobiologie de la Méditerranée, Inserm U901, Université de la Méditerranée, 13273 Marseille cedex 9, France.
Cattani
Adriano
A
Ackman
James B
JB
Bonifazi
Paolo
P
Aniksztejn
Laurent
L
Ben-Ari
Yehezkel
Y
Cossart
Rosa
R
D000818:Animals; D000831:Animals, Newborn; D001683:Biological Clocks / Q000502:physiology*; D020013:Calcium Signaling / Q000502:physiology; D003344:Cortical Synchronization; D045604:Extracellular Fluid / Q000378:metabolism; D018698:Glutamic Acid / Q000378:metabolism; D002534:Hypoxia, Brain / Q000378:metabolism / Q000503:physiopathology; D008564:Membrane Potentials / Q000502:physiology; D009415:Nerve Net / Q000166:cytology / Q000254:growth & development*; D055495:Neurogenesis / Q000502:physiology*; D009924:Organ Culture Techniques; D051381:Rats; D017208:Rats, Wistar; D016194:Receptors, N-Methyl-D-Aspartate / Q000378:metabolism; D013003:Somatosensory Cortex / Q000166:cytology / Q000254:growth & development*; D013569:Synapses / Q000502:physiology* / Q000648:ultrastructure; D055366:Synaptic Potentials / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D016194:Receptors, N-Methyl-D-Aspartate; D018698:Glutamic Acid; D005680:gamma-Aminobutyric Acid