Elsevier

NeuroImage

Volume 62, Issue 4, 1 October 2012, Pages 2212-2221
NeuroImage

Review
Spontaneous activity in developing sensory circuits: Implications for resting state fMRI

https://doi.org/10.1016/j.neuroimage.2012.02.046Get rights and content

Abstract

The immature brain spontaneously expresses unique patterns of electrical activity that are believed to contribute to the development of neuronal networks. Certain electrographic features of this activity, particularly modulation on an infraslow time scale, resemble activity patterns observed in the mature brain at ‘rest’, loosely defined as the absence of an investigator imposed task. However, it is not clear whether the immature activity patterns observed at rest are precursors of the spontaneous neuronal activity that forms resting state networks in the adult. Here, we review recent studies that have explored the generative mechanisms of resting state activity during development in the primary sensory systems of premature human neonates and neonatal rodents. The remarkable hypothesis suggested by this work is that while resting state activity during the pre- and possibly near-term period can bear superficial resemblance to adult activity it is fundamentally different in terms of function and origin. During early development spontaneous thalamocortical activity in primary sensory regions is determined largely by transitory generators in the sensory periphery. This is in contrast to the adult, where spontaneous activity generated within thalamocortex, particularly by cortico-cortical connections, dominates. We therefore suggest a conservative interpretation of developmental mapping studies which are based on indirect measurement of activity (e.g. fMRI), or on the partitioning of EEG frequency using bands derived from adult studies. The generative mechanisms for brain activity at early ages are likely different from those of adults, and may play very different roles; for example in circuit formation as opposed to attention.

Section snippets

Resting state activity in neonates and adults

The cerebral cortex is never quiet (Fox and Raichle, 2007). Even primary sensory regions are consistently active in the absence of sensory input, including during states of unconsciousness such as non-REM sleep and anesthesia (Bianciardi et al., 2009, Hasenstaub et al., 2007, Leopold and Logothetis, 2003). Neurophysiologists have a tradition of labeling such non-task related activity ‘spontaneous’ or even ‘background’, while similar fluctuations have been categorized as ‘resting state’ by the

Discontinuous temporal organization of early activity

The adult brain is constantly active, though the patterns and amount of this activity are modulated differentially between brain networks by a number of factors including vigilance state, mental task and sensory input (Steriade and McCarley, 2005). The basis of functional connectivity mapping appears to be the waxing and waning of ongoing activity on an ‘infraslow’ timescale (0.01–0.2 Hz), rather than the cessation and re-induction of activity itself (Baria et al., 2011, Jann et al., 2010, Laufs

Unique activity patterns in preterm infants

We have considered the differences in the nature of the infraslow oscillations observed at rest during early development and in adults, namely the alternation between network silence and activity that characterizes the immature brain, as opposed to waxing and waning of continuous activity in the adult. The next question is whether the activity bursts that interrupt network silences are fragments of the cortico-cortical activity that composes the adult resting state, or are of a qualitatively

Peripheral dominance of resting activity during early development

Investigators have used the somatosensory and visual cortex of rats and ferrets to ask the following question: Is resting activity in neonates driven by cortico-cortical connections as it is in adults, or is it driven by other mechanisms such as spontaneous activity in the sense organ? These studies have revealed that the large majority of cortical activity during the period of discontinuity results from input generated spontaneously at the sensory periphery, not within cortex. Examination of

Development of intrinsic thalamocortical activities

If the basis of resting state activity modulations in sensory cortex during early development is spontaneous activation at the periphery, then they result from different functional circuits from those generating resting activity in the adult. The activity patterns most closely associated with resting state modulations in sensory cortex are delta waves (Jann et al., 2010, Lu et al., 2007), which result from spontaneous activation of thalamocortical circuits during sleep or periods of low

Early cortical function and implications for resting state fMRI

We have presented evidence that ‘resting state’ modulations of activity in sensory cortex during early ages are not the same infraslow modulation present in the adult. This is supported by two characteristics of neocortical activity during the fetal and early neonatal period (1) unique early network activities driven by the sensory periphery and (2) the lack of intrinsic activity generated in thalamocortical circuits. The young resting state activities represent a unique network state that is

Summary

Electrophysiological evidence in human preterm infants and animal models reviewed here is consistent with the hypothesis that early circuit development is characterized by a unique state of cortical network dynamics, in which adult-like thalamocortical resting state activity is minimal, allowing inputs from the periphery to be amplified by cortical oscillatory bursts (Fig. 3). This period appears tightly regulated to coincide with the sensory deprivation experienced in the womb (or maintained

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