Decreases in Energy and Increases in Phase Locking of Event-Related Oscillations to Auditory Stimuli Occur during Adolescence in Human and Rodent Brain

Ehlers, Cindy L.; Wills, Derek N.; Desikan, Anita; Phillips, Evelyn; Havstad, James W.

doi:10.1159/000358484

Cited by 26 publications

(22 citation statements)

References 120 publications

(114 reference statements)

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“…In particular, even after accounting for the effects of volume conduction on brain electric signals, the density and spatial variability of alpha-band cortical networks increased in late childhood – this trend likely continues to mature into young adulthood (Uhlhaas et al, 2010). Taken together, these findings are consistent with evidence demonstrating that the maturing brain is characterized by an enhanced ability to maintain phase synchronized brain oscillations within specific frequency ranges (Ehlers et al, 2014; Poulsen, Picton, & Paus, 2009; Uhlhaas et al, 2009). The ability to sustain precise patterns of neuronal coordination ( i.e.…”

Section: Discussionsupporting

confidence: 89%

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

et al. 2015

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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 more 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 towards 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.

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Section: Discussionsupporting

confidence: 89%

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

et al. 2015

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“…The S -transform magnitude squared for a time/frequency interval is therefore proportional to volts squared. These analyses are similar to what has been previously described (Ehlers et al, 2014). …”

Section: 0 Methodssupporting

confidence: 87%

Low voltage alpha EEG phenotype is associated with reduced amplitudes of alpha event-related oscillations, increased cortical phase synchrony, and a low level of response to alcohol

Ehlers

Wills

Phillips

et al. 2015

International Journal of Psychophysiology

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Low voltage EEG (LVEEG) is a heritable phenotype that differs depending on ancestral heritage, yet its impact on brain networks and cognition remain relatively unexplored. In this study we assessed energy and task related phase locking of event-related oscillation (EROs), behavioral responses, measures of IQ and personality, and expected responses to alcohol in a large sample of individuals with LVEEG compared to those with higher voltage variants. Participants (n=762) were recruited from a Native American community and completed a diagnostic interview, the Quick Test, the Subjective High Assessment Scale Expectation Version (SHAS-E) and the Maudsley Personality Inventory. Clinical and spectral analyzed EEGs were collected for determination of the presence of a LVEEG variant. EROs were generated using a facial expression recognition task. Participants with LVEEG (n=451) were significantly more likely to be older, married and have higher degrees of Native American heritage but did not differ in gender, income or education. Individuals with LVEEG were also found to have decreased energy in their alpha EROs, increased phase locking between stimulus trials, and increased phase-locking between cortical brain areas. No significant differences in the cognitive tests, personality variables or alcohol dependence or anxiety diagnoses were found, however, individuals with LVEEG did report a larger number of drinks ever consumed in a 24-hr period and a less intense expected response to alcohol. These data suggest that alpha power in the resting EEG is highly associated with energy and cortical connectivity measures generated by event-related stimuli, as well as potentially increased risk for alcohol use.

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“…For example, Gaetz et al(64) observed greater movement-related motor cortex gamma synchrony in adolescent (11- to 13-years-old) versus younger children (4- to 6-years-old), suggesting a more general phenomena. Maturation of neural oscillatory activity is, of course, observed in frequencies below gamma (e.g., (65-67)), with a recent translational study (human and rat) suggesting that increased neural synchrony may be a general feature of neural network maturation(68). …”

Section: Discussionmentioning

confidence: 99%

Translating Adult Electrophysiology Findings to Younger Patient Populations: Difficulty Measuring 40-Hz Auditory Steady-State Responses in Typically Developing Children and Children with Autism Spectrum Disorder

Edgar

th²,

S³

et al. 2016

Dev Neurosci

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Background: γ (∼30-80 Hz) brain rhythms are thought to be abnormal in neurodevelopmental disorders such as schizophrenia and autism spectrum disorder (ASD). In adult populations, auditory 40-Hz click trains or 40-Hz amplitude-modulated tones are used to assess the integrity of superior temporal gyrus (STG) 40-Hz γ-band circuits. As STG 40-Hz auditory steady-state responses (ASSRs) are not fully developed in children, tasks using these stimuli may not be optimal in younger patient populations. The present study examined this issue in typically developing (TD) children as well as in children with ASD, using source localization to directly assess activity in the principal generators of the 40-Hz ASSR in the left and right primary/secondary auditory cortices. Methods: 40-Hz amplitude-modulated tones of 1 s duration were binaurally presented while magnetoencephalography data were obtained from 48 TD children (45 males; 7-14 years old) and 42 ASD children (38 males; 8-14 years old). T1-weighted structural MRI was obtained. Using single dipoles anatomically constrained to each participant's left and right Heschl's Gyrus, left and right 40-Hz ASSR total power (TP) and intertrial coherence (ITC) measures were obtained. Associations between 40-Hz ASSR TP, ITC and age as well as STG gray matter cortical thickness (CT) were assessed. Group STG function and structure differences were also examined. Results: TD and ASD did not differ in 40-Hz ASSR TP or ITC. In TD and ASD, age was associated with left and right 40-Hz ASSR ITC (p < 0.01). The interaction term was not significant, indicating in both groups a ∼0.01/year increase in ITC. 40-Hz ASSR TP and ITC were greater in the right than left STG. Groups did not differ in STG CT, and no associations were observed between 40-Hz ASSR activity and STG CT. Finally, right STG transient γ (50-100 ms and 30-50 Hz) was greater in TD versus ASD (significant for TP, trend for ITC). Conclusions: The 40-Hz ASSR develops, in part, via an age-related increase in neural synchrony. Greater right than left 40-Hz ASSRs (ITC and TP) suggested earlier maturation of right versus left STG neural network(s). Given a ∼0.01/year increase in ITC, 40-Hz ASSRs were weak or absent in many of the younger participants, suggesting that 40-Hz driving stimuli are not optimal for examining STG 40-Hz auditory neural circuits in younger populations. Given the caveat that 40-Hz auditory steady-state neural networks are poorly assessed in children, the present analyses did not point to atypical development of STG 40-Hz ASSRs in higher-functioning children with ASD. Although groups did not differ in 40-Hz auditory steady-state activity, replicating previous studies, there was evidence for greater right STG transient γ activity in TD versus ASD.

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Decreases in Energy and Increases in Phase Locking of Event-Related Oscillations to Auditory Stimuli Occur during Adolescence in Human and Rodent Brain

Cited by 26 publications

References 120 publications

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

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

Low voltage alpha EEG phenotype is associated with reduced amplitudes of alpha event-related oscillations, increased cortical phase synchrony, and a low level of response to alcohol

Translating Adult Electrophysiology Findings to Younger Patient Populations: Difficulty Measuring 40-Hz Auditory Steady-State Responses in Typically Developing Children and Children with Autism Spectrum Disorder

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