A transient postnatal quiescent period precedes emergence of mature cortical dynamics.

Mature neural networks synchronize and integrate spatiotemporal activity patterns to support cognition. Emergence of these activity patterns and functions is believed to be developmentally regulated, but the postnatal time course for neural networks to perform complex computations remains unknown. We investigate the progression of large-scale synaptic and cellular activity patterns across development using high spatiotemporal resolution in vivo electrophysiology in immature mice. We reveal that mature cortical processes emerge rapidly and simultaneously after a discrete but volatile transition period at the beginning of the second postnatal week of rodent development. The transition is characterized by relative neural quiescence, after which spatially distributed, temporally precise, and internally organized activity occurs. We demonstrate a similar developmental trajectory in humans, suggesting an evolutionarily conserved mechanism that could facilitate a transition in network operation. We hypothesize that this transient quiescent period is a requisite for the subsequent emergence of coordinated cortical networks. It can take several months, or even years, for the brain of a young animal to develop and refine the complex neural networks which underpin cognitive abilities such as memory, planning, and decision making. While the properties that support these functions have been well-documented, less is known about how they emerge during development. Domínguez, Ma, Yu et al. therefore set out to determine when exactly these properties began to take shape in mice, using lightweight nets of electrodes to record brain activity in sleeping newborn pups. The nets were designed to avoid disturbing the animals or damaging their fragile brains. The recordings showed that patterns of brain activity similar to those seen in adults emerged during the first couple of weeks after birth. Just before, however, the brains of the pups went through a brief period of reduced activity: this lull seemed to mark a transition from an immature to a more mature mode of operation. After this pause, neurons in the mouse brains showed coordinated patterns of firing reminiscent of those seen in adults. By monitoring the brains of human babies using scalp sensors, Domínguez, Ma, Yu et al. showed that a similar transition also occurs in infants during their first few months of life, suggesting that brains may mature via a process retained across species. Overall, the relative lull in activity before transition may mark when neural networks gain mature properties; in the future, it could therefore potentially be used to diagnose and monitor individuals with delayed cognitive development.

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© 2021, Domínguez et al.

Déclaration de conflit d'intérêts

SD, LM, HY, GP, CM, GS, CC, GB, GF, DK, JG No competing interests declared