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  • Review Article
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Network state transitions during cortical development

Abstract

Mammalian cortical networks are active before synaptogenesis begins in earnest, before neuronal migration is complete, and well before an animal opens its eyes and begins to actively explore its surroundings. This early activity undergoes several transformations during development. The most important of these is a transition from episodic synchronous network events, which are necessary for patterning the neocortex into functionally related modules, to desynchronized activity that is computationally more powerful and efficient. Network desynchronization is perhaps the most dramatic and abrupt developmental event in an otherwise slow and gradual process of brain maturation. In this Review, we summarize what is known about the phenomenology of developmental synchronous activity in the rodent neocortex and speculate on the mechanisms that drive its eventual desynchronization. We argue that desynchronization of network activity is a fundamental step through which the cortex transitions from passive, bottom–up detection of sensory stimuli to active sensory processing with top–down modulation.

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Fig. 1: In vivo cortical network state transitions across development.
Fig. 2: Thalamocortical influences on cortical network activity during development.
Fig. 3: Mechanisms of desynchronization and other network transitions.

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Acknowledgements

We are grateful to M. Colonnese, M. Dipoppa and C. Lohmann for feedback on earlier versions of this manuscript. When citing papers, we attempted to be as inclusive as possible in acknowledging the many investigators whose work has helped shape our ideas; however, we recognize that we have probably missed attributing credit in some cases, and we apologize for any inadvertent oversights. This work was supported by the following grants: Department of Defense (DOD, 13196175), R01NS117597 (NIH-NINDS), R01HD108370 and R01HD054453 (NIH-NICHD) awarded to C.P.-C., by a fellowship grant from the FRAXA research foundation to N.K., and by the Training Grant in Neurobehavioral Genetics (T32NS048004; NIH, NINDS) and the UCLA-Caltech Medical Scientist Training Program (T32 GM008042; NIH, NIGMS) to M.W.W.

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Glossary

Early network oscillations

(ENOs). Synchronous network events recorded in vitro using calcium imaging in the hippocampus and neocortex during the first postnatal week and driven by glutamatergic neurotransmission.

GABAergic calcium events

(GCEs). Synchronous calcium events specifically involving GABAergic interneurons.

Gap junctions

Structures consisting of heteromeric connexin channels in the plasma membrane that form direct conduits between adjacent cells and allow the rapid exchange of small molecules between neighbouring neurons; they are responsible for the dye coupling phenomenon observed in whole cell patch clamp recordings in acute brain slices.

Giant depolarizing potentials

(GDPs). Spontaneous network-mediated synaptic events observed in vitro in the developing hippocampus that are driven by GABAergic neurotransmission.

Neural oscillations

Emergent phenomena of brain circuits that reflect the rhythmic or repetitive firing patterns of groups of neurons. Oscillations can occur spontaneously or in response to sensory stimuli, and they often reflect the interaction between excitation and inhibition.

Neuronal domains

Gap junction-mediated calcium signals that appear synchronously across small clusters of neighbouring neurons in acute brain slices from the neocortex; they are not mediated by action potentials, and it is unclear whether they occur in vivo.

Patchwork SNA

The predominant pattern of SNA seen between E18 and P7 in the rodent neocortex. In patchwork SNA, largely non-overlapping well-circumscribed clusters or patches of neurons fire synchronously, with their firing being separated in time by long periods of quiescence.

Sparsification

A process occurring alongside desynchronization, in which the network activity transitions to a state in which relatively few neurons within the population are firing at any given time.

Spindle bursts

A specific pattern of spontaneous neural activity observed in the immature cortex using electrophysiology that is characterized by a fast oscillatory component (approximately 4–20 Hz) occurring on top of a slower delta wave. Spindle bursts are brief (<2 s) and reflect the synchronous firing of many neurons.

Synchronous network activity

(SNA). Synchronous activity occurring during development that is mediated by chemical synapses and involves most of the neurons within a local network, manifesting either as brief (<3 s) bursts of activity within clusters of neighbouring cells or as larger events that propagate locally within a cortical region.

Up states

Stable depolarized states of the resting membrane potential (Vm) during which action potentials may occur. They are brief (<2 s) and separated by periods when the Vm is more hyperpolarized (Down state) and action potentials do not tend to occur. Transitions between Up and Down states are seen during sleep or quiet wakefulness.

Wave-like SNA

The main pattern of SNA observed in rodent neocortex during the second postnatal week. Wave-like SNA involves large, partially overlapping neuronal ensembles and the activity propagates haltingly, between short periods of quiescence.

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Wu, M.W., Kourdougli, N. & Portera-Cailliau, C. Network state transitions during cortical development. Nat. Rev. Neurosci. 25, 535–552 (2024). https://doi.org/10.1038/s41583-024-00824-y

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