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Resting-state EEG oscillatory dynamics in fragile X syndrome: abnormal functional connectivity and brain network organization.

van der Molen MJ, Stam CJ, van der Molen MW - PLoS ONE (2014)

Bottom Line: A decrease in global functional connectivity was observed in FXS males for upper alpha and beta frequency bands.For theta oscillations, we found increased connectivity in long-range (fronto-posterior) and short-range (frontal-frontal and posterior-posterior) clusters.These findings are discussed in terms of aberrant maturation of neuronal oscillatory dynamics, resulting in an imbalance in excitatory and inhibitory neuronal circuit activity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Psychology, Developmental Psychology Unit, Leiden University, Leiden, the Netherlands ; Leiden Institute for Brain and Cognition. Leiden, the Netherlands.

ABSTRACT
Disruptions in functional connectivity and dysfunctional brain networks are considered to be a neurological hallmark of neurodevelopmental disorders. Despite the vast literature on functional brain connectivity in typical brain development, surprisingly few attempts have been made to characterize brain network integrity in neurodevelopmental disorders. Here we used resting-state EEG to characterize functional brain connectivity and brain network organization in eight males with fragile X syndrome (FXS) and 12 healthy male controls. Functional connectivity was calculated based on the phase lag index (PLI), a non-linear synchronization index that is less sensitive to the effects of volume conduction. Brain network organization was assessed with graph theoretical analysis. A decrease in global functional connectivity was observed in FXS males for upper alpha and beta frequency bands. For theta oscillations, we found increased connectivity in long-range (fronto-posterior) and short-range (frontal-frontal and posterior-posterior) clusters. Graph theoretical analysis yielded evidence of increased path length in the theta band, suggesting that information transfer between brain regions is particularly impaired for theta oscillations in FXS. These findings are discussed in terms of aberrant maturation of neuronal oscillatory dynamics, resulting in an imbalance in excitatory and inhibitory neuronal circuit activity.

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Related in: MedlinePlus

Mean normalized path length over all epochs for FXS and controls participants in the delta (0.05–4 Hz), theta (4–8 Hz), lower alpha (8–10 Hz), upper alpha (10–13 Hz), beta (13–30 Hz), and gamma (30–45 Hz) frequency range.Path length in the theta band is significant longer in FXS males as compared to controls. Asterisks represent significant differences at p<.05. Error bars represent standard error of the mean.
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pone-0088451-g005: Mean normalized path length over all epochs for FXS and controls participants in the delta (0.05–4 Hz), theta (4–8 Hz), lower alpha (8–10 Hz), upper alpha (10–13 Hz), beta (13–30 Hz), and gamma (30–45 Hz) frequency range.Path length in the theta band is significant longer in FXS males as compared to controls. Asterisks represent significant differences at p<.05. Error bars represent standard error of the mean.

Mentions: Figures 4 and 5 depict the normalized weighted clustering coefficients and normalized weighted path length, respectively, for FXS males and controls. Local segregation as represented by the clustering coefficient did not differ significantly between the groups (Figure 4). A decrease of the clustering coefficient is typically interpreted to reflect local connection loss, whereas an increase may reflect increased connectivity [48]. For normalized path length, larger normalized path length was observed for the theta spectral band in FXS individuals relative to controls, t(18) = 2.70, p = 0.02, ηp2 = .29. The small-world index S for all spectral bands (except for gamma) was smaller in FXS than controls but these differences were not significant (see Table 1). This suggests that brain networks in FXS still display small-world properties. However, the differences in path length for the theta band, shows that global information transfer within the network may be particularly compromised in neuronal networks that govern theta oscillatory activity. This finding could mirror the excess of neuronal connections found in neurobiological studies [9] and could compromise the efficiency of information transfer within the network. This notion is in line with our present connectivity results and previous findings of augmented theta power activity in FXS individuals [27]. Notably, the current network parameters are not likely to be confounded by spectral power or PLI, as the normalized path length and clustering coefficients were compared to its surrogate networks indices [37].


Resting-state EEG oscillatory dynamics in fragile X syndrome: abnormal functional connectivity and brain network organization.

van der Molen MJ, Stam CJ, van der Molen MW - PLoS ONE (2014)

Mean normalized path length over all epochs for FXS and controls participants in the delta (0.05–4 Hz), theta (4–8 Hz), lower alpha (8–10 Hz), upper alpha (10–13 Hz), beta (13–30 Hz), and gamma (30–45 Hz) frequency range.Path length in the theta band is significant longer in FXS males as compared to controls. Asterisks represent significant differences at p<.05. Error bars represent standard error of the mean.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3921158&req=5

pone-0088451-g005: Mean normalized path length over all epochs for FXS and controls participants in the delta (0.05–4 Hz), theta (4–8 Hz), lower alpha (8–10 Hz), upper alpha (10–13 Hz), beta (13–30 Hz), and gamma (30–45 Hz) frequency range.Path length in the theta band is significant longer in FXS males as compared to controls. Asterisks represent significant differences at p<.05. Error bars represent standard error of the mean.
Mentions: Figures 4 and 5 depict the normalized weighted clustering coefficients and normalized weighted path length, respectively, for FXS males and controls. Local segregation as represented by the clustering coefficient did not differ significantly between the groups (Figure 4). A decrease of the clustering coefficient is typically interpreted to reflect local connection loss, whereas an increase may reflect increased connectivity [48]. For normalized path length, larger normalized path length was observed for the theta spectral band in FXS individuals relative to controls, t(18) = 2.70, p = 0.02, ηp2 = .29. The small-world index S for all spectral bands (except for gamma) was smaller in FXS than controls but these differences were not significant (see Table 1). This suggests that brain networks in FXS still display small-world properties. However, the differences in path length for the theta band, shows that global information transfer within the network may be particularly compromised in neuronal networks that govern theta oscillatory activity. This finding could mirror the excess of neuronal connections found in neurobiological studies [9] and could compromise the efficiency of information transfer within the network. This notion is in line with our present connectivity results and previous findings of augmented theta power activity in FXS individuals [27]. Notably, the current network parameters are not likely to be confounded by spectral power or PLI, as the normalized path length and clustering coefficients were compared to its surrogate networks indices [37].

Bottom Line: A decrease in global functional connectivity was observed in FXS males for upper alpha and beta frequency bands.For theta oscillations, we found increased connectivity in long-range (fronto-posterior) and short-range (frontal-frontal and posterior-posterior) clusters.These findings are discussed in terms of aberrant maturation of neuronal oscillatory dynamics, resulting in an imbalance in excitatory and inhibitory neuronal circuit activity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Psychology, Developmental Psychology Unit, Leiden University, Leiden, the Netherlands ; Leiden Institute for Brain and Cognition. Leiden, the Netherlands.

ABSTRACT
Disruptions in functional connectivity and dysfunctional brain networks are considered to be a neurological hallmark of neurodevelopmental disorders. Despite the vast literature on functional brain connectivity in typical brain development, surprisingly few attempts have been made to characterize brain network integrity in neurodevelopmental disorders. Here we used resting-state EEG to characterize functional brain connectivity and brain network organization in eight males with fragile X syndrome (FXS) and 12 healthy male controls. Functional connectivity was calculated based on the phase lag index (PLI), a non-linear synchronization index that is less sensitive to the effects of volume conduction. Brain network organization was assessed with graph theoretical analysis. A decrease in global functional connectivity was observed in FXS males for upper alpha and beta frequency bands. For theta oscillations, we found increased connectivity in long-range (fronto-posterior) and short-range (frontal-frontal and posterior-posterior) clusters. Graph theoretical analysis yielded evidence of increased path length in the theta band, suggesting that information transfer between brain regions is particularly impaired for theta oscillations in FXS. These findings are discussed in terms of aberrant maturation of neuronal oscillatory dynamics, resulting in an imbalance in excitatory and inhibitory neuronal circuit activity.

Show MeSH
Related in: MedlinePlus