Decreases in energy and increases in phase locking of event-related oscillations to auditory stimuli occur during adolescence in human and rodent brain.

paper Cited Public

Authors: Ehlers, Cindy L; Wills, Derek N; Desikan, Anita; Phillips, Evelyn; Havstad, James
Year: 2014
Journal: Developmental neuroscience
PMID: 24819672
DOI: 10.1159/000358484
PMCID: PMC4125510

Synchrony of phase (phase locking) of event-related oscillations (EROs) within and between different brain areas has been suggested to reflect communication exchange between neural networks and as such may be a sensitive and translational measure of changes in brain remodeling that occur during adolescence. This study sought to investigate developmental changes in EROs using a similar auditory event-related potential (ERP) paradigm in both rats and humans. Energy and phase variability of EROs collected from 38 young adult men (aged 18-25 years), 33 periadolescent boys (aged 10-14 years), 15 male periadolescent rats [at postnatal day (PD) 36] and 19 male adult rats (at PD103) were investigated. Three channels of ERP data (frontal cortex, central cortex and parietal cortex) were collected from the humans using an 'oddball plus noise' paradigm that was presented under passive (no behavioral response required) conditions in the periadolescents and under active conditions (where each subject was instructed to depress a counter each time he detected an infrequent target tone) in adults and adolescents. ERPs were recorded in rats using only the passive paradigm. In order to compare the tasks used in rats to those used in humans, we first studied whether three ERO measures [energy, phase locking index (PLI) within an electrode site and phase difference locking index (PDLI) between different electrode sites] differentiated the 'active' from 'passive' ERP tasks. Secondly, we explored our main question of whether the three ERO measures differentiated adults from periadolescents in a similar manner in both humans and rats. No significant changes were found in measures of ERO energy between the active and passive tasks in the periadolescent human participants. There was a smaller but significant increase in PLI but not PDLI as a function of active task requirements. Developmental differences were found in energy, PLI and PDLI values between the periadolescents and adults in both the rats and the human participants. Neuronal synchrony as indexed by PLI and PDLI was significantly higher to the infrequent (target) tone compared to the frequent (nontarget) tone in all brain sites in all of the regions of interest time-frequency intervals. Significantly higher ERO energy and significantly lower synchrony was seen in the periadolescent humans and rats compared to their adult counterparts. Taken together these findings are consistent with the hypothesis that adolescent remodeling of the brain includes decreases in energy and increases in synchrony over a wide frequency range both within and between neuronal networks and that these effects are conserved over evolution.

Figure 1

Grand mean values for energy, phase locking index (PLI) and phase difference lock index (PDLI) of event-related oscillations for the passive and active task in periadolescents. (a) MANOVA revealed that the infrequent (target) tone (white bars), as compared to the frequent (non-target) tone (black bars), produced no significant differences in energy by tone or between passive and active task. (b) PLI was significantly increased following the infrequent tone compared to the frequent tone [** indicates p<0.001] and was decreased in the active task [+ indicates p<0.007]. (c) PDLI was also significantly increased following the infrequent tone but not different between the tasks. Error Bars = S.E.M

Figure 2

Significant mean values for energy of event-related oscillations (EROs) following the infrequent (target) tone for periadolescents (white bars) and adults (black bars) in the delta (1-4 Hz, 200-500 ms), theta (4-7 Hz 10-400 ms), alpha (7-13 Hz, 0-300 ms), and beta (13-30 Hz, 0-300 ms) time-frequency ranges for the three electrode locations in the humans (a) (periadolescent n=19, adult n=38) (FZ=midline frontal cortex, CZ=midline central cortex, PZ=midline parietal cortex) and in the rats (b) (periadolescent n=15, adult n=19) (FCTX= frontal cortex, PCTX= parietal cortex). Energy in periadolescents, as compared to adults, is significantly higher across most frequency bands and electrode sites in humans and in rats. * indicates p<0.01, ** p<0.001. Error Bars = S.E.M

Figure 3

Grand averages of energy for event–related oscillations (EROs) in humans given the active task (periadolescent n=19, adult n=38). Each graph depicts a time-frequency representation of energy values in periadolescents and adults following the infrequent (target) tone in the three electrode locations (FZ=midline frontal cortex, CZ=midline central cortex, PZ=midline parietal cortex). In each graph, frequency (Hz) is presented on the Y-axis, time regions of interest on the X-axis (msec). Energy is presented as color equivalents as indicated on the bar at the bottom of each graph. Periadolescents compared to adults show overall higher energy across the time-frequencies and in all electrode sites compared to adults.

Figure 4

Significant mean values for the phase lock index (PLI) of event-related oscillations (EROs) following the infrequent (target) tone for periadolescents (white bars) and adults (black bars) for delta (1-4 Hz, 200-500 ms), theta (4-7 Hz 10-400 ms) and alpha (7-13 Hz, 0-300 ms) time-frequency ranges. (a) Human adults (periadolescents n=19, adults n=38) showed significantly higher phase lock index in the delta and theta time-frequencies across all three electrode locations compared to periadolescents. (b) Adult rats (periadolescent n=15, adult n=19) showed a significant decrease in the delta time-frequency in the frontal cortex and an increase in alpha time-frequencies at parietal cortex when compared to periadolescents. * indicates p<0.01, ** p<0.001. Error Bars = S.E.M.

Figure 5

Grand averages of PLI (phase lock index) for event–related oscillations (EROs) in humans given the active task (periadolescent n=19, adult n=38). Each graph depicts a time-frequency representation of phase angle synchrony values in periadolescents and adults following the infrequent (target) tone in the three electrode locations (FZ=midline frontal cortex, CZ=midline central cortex, PZ=midline parietal cortex). In each graph frequency (Hz) is presented on the Y-axis, time regions of interest on the X-axis (msec). PLI is presented as color equivalents as indicated on the bar at the bottom of each graph.

Figure 6

Significant mean values for the phase difference lock index (PDLI) of event-related oscillations (EROs) following the infrequent (target) tone for periadolescent (white bars) and adults (black bars) in the delta (1-4 Hz, 200-500 ms), theta (4-7 Hz 10-400 ms), alpha (7-13 Hz, 0-300 ms), and beta (13-30 Hz, 0-300 ms) time-frequency ranges. Phase differences were calculated between midline frontal cortex (FZ) and midline parietal cortex (PZ) for the human study and between frontal cortex (FCTX) and parietal cortex (PCTX) in the rats. (a) Human adults showed significantly increased PDLI across all frequency bands when compared to periadolescents. (b) Adult rats (periadolescent n=14, adult n=18) also had significant increases in PDLI in the theta, alpha and beta time-frequencies. * indicates p<0.01, ** p<0.001. Error Bars = S.E.M.

Figure 7

Grand averages of energy for event–related oscillations (EROs) in rats (periadolescents n=13, adults n=18). Each graph depicts a time-frequency representation of energy values in periadolescent and adult rats following the infrequent (target) tone in two electrode locations (FCTX=frontal cortex, PCTX=parietal cortex). In each graph frequency (Hz) is presented on the Y-axis, time regions of interest on the X-axis (msec) and energy is presented as color equivalents as indicated on the bar at the bottom of each graph. Periadolescent rats show greater energy across the time-frequencies and in both electrode sites when compared to adult rats.

Figure 8

Grand averages of PLI (phase lock index) for event–related oscillations (EROs) in rats (periadolescents n=13, adults n=18). Each graph depicts a time-frequency representation of phase angle synchrony in adolescent and adult rats following the infrequent (target) tone in two electrode locations (FCTX=frontal cortex, PCTX=parietal cortex). In each graph frequency (Hz) is presented on the Y-axis, time regions of interest on the X-axis (msec) and PLI is presented as color equivalents as indicated on the bar at the bottom of each graph.

#	Section	Preview
20	Experimental procedures — ERO, PLI, and PDLI analyses	To reduce anomalies in the S-transform output at the beginning and the end of the output time…
21	Experimental procedures — ERO, PLI, and PDLI analyses	An S transformation at time t and frequency f has real and imaginary parts
22	Experimental procedures — ERO, PLI, and PDLI analyses	where i is the square root of minus 1. The cosine and sine of the phase angle at this time-frequency…
23	Experimental procedures — ERO, PLI, and PDLI analyses	where the vertical bar pair indicates magnitude, here and below. The cosine and sine of phase angle…
24	Experimental procedures — ERO, PLI, and PDLI analyses	PLI is a measure of synchrony of phase angle over trials, as a function of frequency and of time…
25	Experimental procedures — ERO, PLI, and PDLI analyses	where the angle bracket pair indicates mean value over eligible trials, here and below. Eligibility…
26	Experimental procedures — ERO, PLI, and PDLI analyses	PDLI is a measure of constancy over trials of the difference in phase angle between two channels, as…
27	Experimental procedures — ERO, PLI, and PDLI analyses	where ϕA and ϕB are phase angles of channels A and B, respectively. This definition of PDLI is…
28	Experimental procedures — ERO, PLI, and PDLI analyses	Rectangular regions of interest (ROIs) were defined within the time-frequency analysis plane by…
29	Experimental procedures — Statistical analyses	The first set of analyses (IBM SPSS statistics 20.0. Armonk, NY: IBM Corp) were aimed at determining…
30	Experimental procedures — Statistical analyses	if the age of the participants in the active task differed from those in the passive task a one-way…
31	Results	Thirty-eight (38) adult and 31 periadolescent human participants (all males) had valid…
32	Results — ERO responses to frequent and infrequent tones in the “active” and “passive” tasks in periadolescent humans	One-way ANOVA revealed that there were no significant age differences between the periadolescent…
33	Results — ERO responses to frequent and infrequent tones in the “active” and “passive” tasks in periadolescent humans	FZ=54.4 ± 6.8, CZ=64.1 ± 6.8, PZ=88.4 ± 6.8), with the Parietal cortex having higher energy than…
34	Results — ERO responses to frequent and infrequent tones in the “active” and “passive” tasks in periadolescent humans	A highly significant main effect of tone was found in phase difference lock index (PDLI) between FZ…
35	Results — Developmental differences in EROs in humans	The second major research question concerned whether adults differed from periadolescents in ERO…
36	Results — Developmental differences in EROs in humans	As seen in Figure 2a, in the ANOVA revealed that periadolescents also had significantly higher…
37	Results — Developmental differences in EROs in humans	An evaluation of PLI values in the human participants using MANOVA revealed a main effect of group…
38	Results — Developmental differences in EROs in humans	Figure 4a gives the mean (± SE) values for the PLI for each frequency range for the three electrode…
39	Results — Developmental differences in EROs in humans	An evaluation of PDLI values in the human participants for the electrode pair FZ and PZ using MANOVA…

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In this knowledge base

Title	Year	PMID
Gender modulates the development of theta event related oscillations in adolescents and young adults.	2015	26102560

External

Title	Authors	Journal	Year	Link
Accumbens connectivity during deep-brain stimulation differentiates loss of control from physiologic behavioral states.	Rolle CE et al.	—	2023	→
Event-related Oscillations to Emotional Faces are Related to a History of Internalizing Disorders.	Ehlers CL et al.	—	2023	→
Amphetamine alters an EEG marker of reward processing in humans and mice.	Cavanagh JF et al.	—	2022	→
Amphetamine alters an EEG marker of reward processing in humans and mice	Cavanagh JF et al.	—	2021	—
Chronic intermittent ethanol during adolescence and adulthood alters dendritic spines in the primary motor and visual cortex in rats.	Amodeo LR et al.	—	2021	→
Commentary on Wright and Bourke "The growth of cognition: Free energy minimization and the embryogenesis of cortical computation".	Rapp PE	—	2021	→
Differential neurodynamics and connectivity in the dorsal and ventral visual pathways during perception of emotional crowds and individuals: a MEG study.	Im HY et al.	—	2021	→
Electrophysiological biomarkers of behavioral dimensions from cross-species paradigms.	Cavanagh JF et al.	—	2021	→
Multiparity decreases the effect of distractor stimuli on a working memory task: An EEG study.	M PH et al.	—	2021	→
Delta Event-Related Oscillations Are Related to a History of Extreme Binge Drinking in Adolescence and Lifetime Suicide Risk.	Ehlers CL et al.	—	2020	→
Phase locking of event-related oscillations is decreased in both young adult humans and rats with a history of adolescent alcohol exposure.	Ehlers CL et al.	—	2020	→
CR-19-0950: Event-related responses to alcohol-related stimuli in Mexican-American young adults: Relation to age, gender, comorbidity and "dark side" symptoms.	Ehlers CL et al.	—	2019	→
Mechanisms of Persistent Neurobiological Changes Following Adolescent Alcohol Exposure: NADIA Consortium Findings.	Crews FT et al.	—	2019	→
Developmental trajectory of mismatch negativity and visual event-related potentials in healthy controls: Implications for neurodevelopmental vs. neurodegenerative models of schizophrenia.	Corcoran CM et al.	—	2018	→
Novelty N2-P3a Complex and Theta Oscillations Reflect Improving Neural Coordination Within Frontal Brain Networks During Adolescence.	Wienke AS et al.	—	2018	→
Acute dosing of vortioxetine strengthens event-related brain activity associated with engagement of attention and cognitive functioning in rats.	Laursen B et al.	—	2017	→
Alcohol drinking during adolescence increases consumptive responses to alcohol in adulthood in Wistar rats.	Amodeo LR et al.	—	2017	→
Listening to a baby crying induces higher electroencephalographic synchronization among prefrontal, temporal and parietal cortices in adoptive mothers.	Pérez-Hernández M et al.	—	2017	→
Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior.	Crews FT et al.	—	2016	→
Event-related oscillations (ERO) during an active discrimination task: Effects of lesions of the nucleus basalis magnocellularis.	Sanchez-Alavez M et al.	—	2016	→
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 JC et al.	—	2016	→
Developmental changes in spontaneous electrocortical activity and network organization from early to late childhood.	Miskovic V et al.	—	2015	→
Gender modulates the development of theta event related oscillations in adolescents and young adults.	Chorlian DB et al.	—	2015	→
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 CL et al.	—	2015	→