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Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood.

ABSTRACT: We investigated the development of spontaneous (resting state) cerebral electric fields and their network organization from early to late childhood in a large community sample of children. Critically, we examined electrocortical maturation across one-year windows rather than creating aggregate averages that can miss subtle maturational trends. We implemented several novel methodological approaches including a more fine grained examination of spectral features across multiple electrodes, the use of phase-lagged functional connectivity to control for the confounding effects of volume conduction and applying topological network analyses to weighted cortical adjacency matrices. Overall, there were major decreases in absolute EEG spectral density (particularly in the slow wave range) across cortical lobes as a function of age. Moreover, the peak of the alpha frequency increased with chronological age and there was a redistribution of relative spectral density toward the higher frequency ranges, consistent with much of the previous literature. There were age differences in long range functional brain connectivity, particularly in the alpha frequency band, culminating in the most dense and spatially variable networks in the oldest children. We discovered age-related reductions in characteristic path lengths, modularity and homogeneity of alpha-band cortical networks from early to late childhood. In summary, there is evidence of large scale reorganization in endogenous brain electric fields from early to late childhood, suggesting reduced signal amplitudes in the presence of more functionally integrated and band limited coordination of neuronal activity across the cerebral cortex.

SUBMITTER: Miskovic V

PROVIDER: S-EPMC4554821 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood.

Miskovic Vladimir V Ma Xinpei X Chou Chun-An CA Fan Miaolin M Owens Max M Sayama Hiroki H Gibb Brandon E BE

NeuroImage 20150607

We investigated the development of spontaneous (resting state) cerebral electric fields and their network organization from early to late childhood in a large community sample of children. Critically, we examined electrocortical maturation across one-year windows rather than creating aggregate averages that can miss subtle maturational trends. We implemented several novel methodological approaches including a more fine grained examination of spectral features across multiple electrodes, the use ...[more]

PMID: 26057595

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Project description:Spatially-organized spontaneous activity is a characteristic feature of developing mammalian sensory systems. However, the transitions of spontaneous-activity spatial organization during development and related mechanisms remain largely unknown. We reported previously that layer 4 (L4) glutamatergic neurons in the mouse barrel cortex exhibit spontaneous activity with a patchwork-type pattern at postnatal day (P)5, which is during barrel formation. In the current work, we revealed that spontaneous activity in mouse barrel-cortex L4 glutamatergic neurons exhibits at least three phases during the first two weeks of postnatal development. Phase I activity has a patchwork-type pattern and is observed not only at P5, but also P1, before barrel formation. Phase II is found at P9, by which time barrel formation is completed, and exhibits broadly synchronized activity across barrel borders. Phase III emerges around P11 when L4-neuron activity is desynchronized. The Phase I activity, but not Phase II or III activity, is blocked by thalamic inhibition, demonstrating that the Phase I to II transition is associated with loss of thalamic dependency. Dominant-negative (DN)-Rac1 expression in L4 neurons hampers the Phase II to III transition. It also suppresses developmental increases in spine density and excitatory synapses of L4 neurons in the second postnatal week, suggesting that Rac1-mediated synapse maturation could underlie the Phase II to III transition. Our findings revealed the presence of distinct mechanisms for Phase I to II and Phase II to III transition. They also highlighted the role of a small GTPase in the developmental desynchronization of cortical spontaneous activity.SIGNIFICANCE STATEMENT Developing neocortex exhibits spatially-organized spontaneous activity, which plays a critical role in cortical circuit development. The features of spontaneous-activity spatial organization and the mechanisms underlying its changes during development remain largely unknown. In the present study, using two-photon in vivo imaging, we revealed three phases (Phases I, II, and III) of spontaneous activity in barrel-cortex layer 4 (L4) glutamatergic neurons during the first two postnatal weeks. We also demonstrated the presence of distinct mechanisms underlying phase transitions. Phase I to II shift arose from the switch in the L4-neuron driving source, and Phase II to III transition relied on L4-neuron Rac1 activity. These results provide new insights into the principles of developmental transitions of neocortical spontaneous-activity spatial patterns.

Project description:Early childhood (7-8 years old) and early adolescence (11-12 years old) constitute two landmark developmental stages that comprise considerable changes in neural cognition. However, very limited information from functional neuroimaging studies exists on the functional topological configuration of the human brain during specific developmental periods. In the present study, we utilized continuous resting-state functional near-infrared spectroscopy (rs-fNIRS) imaging data to examine topological changes in network organization during development from early childhood and early adolescence to adulthood. Our results showed that the properties of small-worldness and modularity were not significantly different across development, demonstrating the developmental maturity of important functional brain organization in early childhood. Intriguingly, young children had a significantly lower global efficiency than early adolescents and adults, which revealed that the integration of the distributed networks strengthens across the developmental stages underlying cognitive development. Moreover, local efficiency of young children and adolescents was significantly lower than that of adults, while there was no difference between these two younger groups. This finding demonstrated that functional segregation remained relatively steady from early childhood to early adolescence, and the brain in these developmental periods possesses no optimal network configuration. Furthermore, we found heterogeneous developmental patterns in the regional nodal properties in various brain regions, such as linear increased nodal properties in the frontal cortex, indicating increasing cognitive capacity over development. Collectively, our results demonstrated that significant topological changes in functional network organization occurred during these two critical developmental stages, and provided a novel insight into elucidating subtle changes in brain functional networks across development.

Dataset Information

Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood.

Publications

Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood.

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