Adolescent females exposed to child maltreatment exhibit atypical
EEG coherence and psychiatric impairment: Linking early
adversity, the brain, and psychopathology
VLADIMIR MISKOVIC,aLOUIS A. SCHMIDT,a,bKATHOLIKI GEORGIADES,a,bMICHAEL BOYLE,a,bAND
HARRIET L. MACMILLANa,b
aMcMaster University; andbMcMaster Children’s Hospital
aberrant cortical connectivity of the left hemisphere, no investigations have attempted to examine these relations in the same study. Here, we examined
the links among early adversity, brain connectivity, and functional outcomes. We collected resting regional EEG intra- and interhemispheric a-band
(7.5–12.5 Hz) coherence and measures of general psychiatric impairment from a cohort of 38 adolescent females exposed to child maltreatment (M age ¼
14.47) and 24 adolescent females not exposed to child maltreatment (M age ¼ 14.00). Maltreated youths exhibited more left hemisphere EEG coherence
than the control youths, suggesting a suboptimal organization of cortical networks. Maltreated participants also showed reduced frontal (anterior)
interhemispheric coherence. These differences in brain circuitry remained statistically significant even after controlling for group differences in pubertal
status and socioeconomic status. Measures of functional brain connectivity were associated with several subtypes of abuse and neglect. It was important that
atypical left hemisphere EEG coherence mediated the effects of child maltreatment on levels of psychiatric impairment. The findings are discussed in
the context of models linking early adversity to brain function and psychopathology.
The five major types of child maltreatment (physical, sexual,
emotional abuse, neglect, and exposure to intimate partner
violence) are examples of adverse early life events associated
with a substantial increase in vulnerability for physical health
problems (Danese, Pariante, Caspi, Taylor, & Poulton, 2007;
Felitti et al., 1998) and general psychiatric impairments
(Kessleret al., 1994; MacMillan et al., 2001; Mullen, Martin,
Romans, & Herbison, 1996; Neumann, Houskamp, Pollack,
& Briere, 1996). Functionally, the experience of child mal-
treatment has been linked to multiple negative outcomes,
including threat hypervigilance, depression, impaired self-
regulation, impulsivity, substance abuse, emotional instabil-
ity, interpersonal violence, antisocial tendencies, and border-
line personality disorder (Felitti et al., 1998; Johnson, Cohen,
Brown, Smailes, & Bernstein, 1999; Lewis, 1992; Pollak,
2004, 2005; van der Kolk, 2003; van der Kolk & Fisler, 1994;
sures that can enhance our knowledge of how early adverse
experiences affect brain structure and function (e.g., Curtis
& Cicchetti, 2007). This shift is important, because it is un-
derstood that experience alters complex behavioral outcomes
via its impact on more fundamental brain systems (Knudsen,
2004). One hope is that the addition of biological indices can
help elucidate of the neural bases of risk and resilience, as
well as identify some of the possible mechanisms that are in-
on psychological outcomes (Cicchetti & Valentino, 2006;
Pollak, 2005). An inclusion of multiple levels of analysis
from psychological to biological in a theoretical framework
that does not privilege one over the other promisesto provide
Address correspondence and reprint requests to: Louis A. Schmidt, De-
partment of Psychology, Neuroscience & Behaviour, McMaster University,
Hamilton, ONT L8S 4K1, Canada; E-mail: firstname.lastname@example.org.
This research was supported by grants from the Natural Sciences and Engi-
neering Research Council of Canada (NSERC) and the Social Science and
Humanities Research Council of Canada (to L.S.); a Vanier doctoral scholar-
and Depression,a Faculty Scholar Award from the William T. Grant Founda-
tion, and the Wyeth Canadian Institutes of Health Research (CIHR) Clinical
Research Chair in Women’s Mental Health (to H.M). Further support was
provided by the CIHR Institutes of Gender and Health; Aging; Human De-
velopment, Child and Youth Health; Neurosciences; Mental Health and Ad-
diction; and Population and Public Health and the Johnson Foundation. We
thank the participants for their cooperation and Lindsay Bennett, Sylvia
Nowakowski, Caroline Parkin, Diane Santesso, Masako Tanaka, and Emily
Vella for their help with data collection and data entry. We are also grateful
to the research assistants and nurses who assisted with this project as well as
the comments of Karen Mathewson and three anonymous reviewers.
Development and Psychopathology 22 (2010), 419–432
#Cambridge University Press, 2010
the most useful insights into developmental psychopathology
(Cicchetti & Tucker, 1994; Rutter & Sroufe, 2000).
worth, & Harlow, 1965; Maestripieri et al., 2006; Sanchez,
Ladd, & Plotsky, 2001) and humans (De Bellis et al., 1999;
Ito, Teicher, Glod, & Ackerman, 1998; Pollak, 2005; Teicher,
Glod, Surrey, & Swett, 2003; Wismer Fries, Ziegler, Kurian,
Jacoris, & Pollak, 2005) indicate that the stress of early abuse
and neglect is associated with altered structure and function of
central nervous system components involved in socioaffective
regulation. The most consistent neurobiological correlates of
et al., 1993), dysregulated hypothalamic–pituitary–adrenal
responding (Heim et al., 2000; MacMillan et al., 2009; Ta-
rullo & Gunnar, 2006), and reduced hippocampal and corpus
callosum volumes (Bremner et al., 1997; De Bellis et al., 1999,
2002; Stein, 1997; Teicher et al., 2004). At the level of the neo-
cortex, common neurological impairments associated with mal-
treatment include deficient hemispheric integration (Schiffer,
Teicher, & Papanicolaou, 1995) and left hemisphere electro-
stellation of structural and functional psychobiological changes
initiated by maltreatment has been conceptualized as an envi-
ronmentally induced complex developmental disorder (De Bel-
lis, 2001). The ability to noninvasively index some of the rele-
vant psychobiological processes in developmental populations
provides a viable strategy for bridging the gap between early
experience, brain, and behavior.
EEG Coherence in the Study of Brain Development
One way to assess neocortical aberrations in children and ado-
lescents who have experienced maltreatment is by the use of
quantitative EEG techniques such as EEG coherence. A major
strength of these techniques is that they are relatively inexpen-
sive and noninvasive to use, making them particularlysuitable
for pediatric populations and developmental research.
In computational terms, EEG coherence represents a cross-
correlation in the frequency domain between spatiallyseparate
neuroelectric signals. Coherence has been suggested to reflect
(Nunez, 1981;Thatcher, Krause, & Hrybyk, 1986). The possi-
ble values of EEG coherence range from 0 to 1. Greater values
(more phase synchrony of oscillations) indicate increased neu-
ronal coupling between brain regions and decreased values
(less phase synchrony) indicate more cortical differentiation.
Changes in coherence probably reflect multiple neurophysio-
logical mechanisms, including axonal sprouting, synapto-
genesis, synaptic pruning, myelination, as well as changes in
pre- and postsynaptic neurotransmitter dynamics (Thatcher,
1992). Unfortunately, EEG coherence cannot discriminate be-
tween these distinct physical processes.
cal connections within (intrahemispheric EEG coherence)
spheres. Intrahemispheric corticocortical connections are sub-
served by white matter fibers that exhibit marked variation in
length, whereas interhemispheric connections are subserved
mostly by corpus callosum fibers (Pogarell et al., 2005;
Thatcher et al., 1986).
developmental changes in brain circuitry (Fox & Bell, 1990;
Thatcher et al., 1986; Thatcher, North, & Biver, 2008). One
of the main findings to emerge from this work is that EEG co-
herence waxes and wanes in cyclical patterns across different
stages of ontogenetic development, and that these cycles
seem tohavefunctional correlatesinthe psychologicaldomain
(Thatcher, 1992). It is important to note, however, that high
EEG coherence values are not necessarily reflective of greater
maturation or optimal cortical organization. Thatcher and col-
leagues (2008) have argued that decreased EEG coherence is
associated with more complex cortical networks that support
improvements in the speed and efficiency of information pro-
cessing. Studies of EEG coherence, intelligence, and cogni-
tion, both with developmental and adult populations, provide
ger, 1987; Silberstein, Song, Nunez, & Park, 2004; Thatcher,
McAlaster, Lester, Horst, & Cantor, 1983; Thatcher, North,
& Biver, 2005). Of interest, decreases in EEG coherence are
fancy (Bell & Fox, 1996), possibly reflecting age-dependent
synaptic pruning. These findings are consistent with reports
that the brain’s average connection density decreases with a
concomitant rise in brain size and complexity, reflecting an in-
creasingly modular architecture (Ringo, 1991).
Given its ability to provide temporally resolved informa-
tion regarding dynamic cortical connectivity, EEG coherence
has been used in a range of clinical populations, including
studies of autism (Coben, Clarke, Hudspeth, & Barry, 2008),
schizophrenia (Wada, Nanbu, Kikuchi, Koshino, & Hashi-
moto, 1998), attention-deficit/hyperactivity disorder (Murias,
Swanson, & Srinivasan, 2006), childhood neglect (Marshall,
Reeb, Fox, Nelson, & Zeanah, 2008), and extremely low birth
weight (Miskovic, Schmidt, Boyle, & Saigal, 2009). Some of
these studies have found measures of EEG coherence to be
more sensitive to between-group differences in brain structure
and function than the traditional measures of EEG spectral
Adverse Early Life Events and EEG Coherence
Ito and colleagues (1998) used intrahemispheric a-band EEG
coherence to measure cortical development in hospitalized
children with severe physical or sexual abuse and their age-
and gender-matched nonabused peers. Compared with their
healthy, nonabused counterparts, children who experienced
maltreatment showed greater overall left hemisphere EEG co-
sphere coherence exceeding that of the right hemisphere. By
contrast, normal children evidenced greater right than left
hemisphere coherence, consistent with other studies (Thatcher
V. Miskovic et al.
of white/gray matter and more axonal association fibers in the
right hemisphere (Gur et al., 1980). Increased left hemisphere
coherence in abused children was interpreted as reflecting a
(Ito et al., 1998). Moreover, these results were corroborated by
findings of a greater prevalence of left hemisphere EEG ab-
normalities (Ito et al., 1993) and left hemisphere deficits on
neuropsychological tasks in abused populations (Navalta, Pol-
cari, Webster, Boghossian, & Teicher, 2006; Teicher et al.,
1997). However, other than the one preliminary study (Ito
ing ofexcessive lefthemispheric EEG coherenceinmaltreated
children using a larger sample size.
EEG coherence in children and adolescents who experienced
maltreatment. Nonhuman animal studies have shown that the
development of both the rodent and primate corpus callosum
is negatively influenced by social adversity (e.g., neglect; Ber-
rebi et al., 1988; Denenberg, 1981; Juraska & Kopcik, 1988;
Sanchez, Hearn, Dung, Rilling, & Herndon, 1998). Similarly,
clinical data from human studies have pointed to a reduction
in areas of the midsaggital corpus callosum in maltreated chil-
dren with (De Bellis et al., 1999, 2002) and without (Teicher
et al., 2004) a diagnosis of posttraumatic stress disorder
correlated with regional corpus callosum area (Pogarell et al.,
nectivity deficits associated with child maltreatment.
The Present Study
ings of excessive left hemisphere coherence in a larger sam-
ple of nonhospitalized adolescent females who were exposed
to one or more types of child maltreatment, including physi-
cal, emotional, and sexual abuse and neglect. Second, we ex-
amined interhemispheric EEG coherence differences be-
tween female adolescents exposed to child maltreatment
and their age- and gender-matched peers. In accordance
with previous evidence of corpus callosum atrophy in mal-
treated children (De Bellis et al., 1999, 2002; Teicher et al.,
abnormalities in interhemispheric connectivity. Third, we
performed exploratory analyses in which we examined asso-
ciations between EEG coherence and the different subtypes
of abuse and neglect. Although different subtypes of abuse
and neglect have been suggested to impact development in
unique ways (Sullivan, Fehon, Andres-Hyman, Lipschitz,
& Grilo, 2006; Teicher et al., 2003), this relation has not
been examined in previous studies, primarily because of the
considerable amount of overlap across the various subtypes
(Manly, Kim, Rogosch, & Cicchetti, 2001). Fourth, we at-
tempted to link individual differences in cortical connectivity
to measures of psychiatric adjustment. Although suggested,
research has not empirically demonstrated that electrophysio-
logical disturbances of the left hemisphere associated with
This latter hypothesis is based on at least two lines of re-
search. First, Davidson et al. (Davidson, 2002; Davidson,
Jackson, & Kalin, 2000) has implicated the left frontal
cortex as exerting the principal inhibitory influence over the
amygdala such that reduced left hemisphere function would
lead to a release of subcortical centers and increased emo-
tional lability as well as a reduced ability to successfully reg-
ulate stress. Studies using positron emission tomography
imaging have demonstrated an inverse relation between the
rate of glucose metabolism in the left anterior cortex and
the amygdala (Abercrombie et al., 1996). Evidence from
functional magnetic resonance imaging (fMRI) likewise im-
plicates left anterior structures in the regulation of affect and
behavior (Johnstone, van Reekum Urry, Kalin, & Davidson,
2007; Ochsner, Bunge, Gross, & Gabrieli, 2002).
Second, on the basis of contralateral inhibition between
the two hemispheres, deficient maturation and development
of one hemisphere may be expected to lead to a dominance
of the opposing cerebral hemisphere. Accordingly, underde-
velopment of the left cerebral hemisphere would be expected
to release the negative affect bias of the right hemisphere, be-
cause of decreased modulatory tone (Kinsbourne & Bem-
porad, 1984). This idea has been demonstrated most recently
in studies using slow frequency repetitive transcranial mag-
netic stimulation (rTMS) to transiently inhibit neural net-
works. The application of rTMS technology allows research-
ersto examine dynamic interactions between the two cerebral
hemispheres. For instance, inactivation of the right prefrontal
cortex leadsto an increase in left frontal brain activity (Schut-
ter, van Honk, d’Alfonso, Postma, & de Haan, 2001) and a
reduced tendency to attend to fearful faces (van Honk,
Schutter, d’Alfonso, Kessels, & de Haan, 2002). By contrast,
inactivation of the left frontal cortex increases attention for
fearful faces (d’Alfonso, van Honk, Hermans, Postma, &
de Haan, 2000). There is also structural MRI evidence in psy-
chiatric patients that volumetric asymmetry involving a
smaller left than right orbitofrontal cortex is related to in-
creased impulsivity and aggression (Antonucci et al., 2006).
Although maturational deficits of one hemisphere are more
subtle than rTMS-induced inactivation or volumetric differ-
ences, it is possible that reduced contralateral inhibition of
the right hemisphere might be associated with an increased
prevalence of difficulties regulating stress and emotion. We
predicted that deficits in left hemisphere development as re-
flected in abnormally elevated intrahemispheric EEG coher-
ence would lead to impoverished regulatory abilities ex-
pressed in higher levels of psychiatric impairment.
To summarize, we tested the following five hypotheses:
1. Adolescents exposed to child maltreatment will show ex-
cessive left hemisphere EEG coherence, replicating pre-
viously published work (Ito et al., 1998).
Atypical EEG coherence in child maltreatment
2. They will also exhibit reduced interhemispheric EEG co-
herence, presumably because of reduced corpus callosum
neglect will be associated with differential patterns of in-
tra- and interhemispheric EEG coherence.
4. Atypical brain activity in the adolescents exposed to child
maltreatment, as reflected in EEG coherence, will predict
5. Left EEG coherence will mediate the relation between ex-
posure to child maltreatment and psychiatric impairment.
Femaleyouths between theages of 12 and 16 fromthree local
child protection agencies (CPAs) qualified for eligibility re-
view in the south central region of Ontario, Canada. Only fe-
males were enrolled because the present study was part of a
larger exploratory study that examined the cortisol response
dictor of subsequent depression (see MacMillan et al., 2009);
because depression istwo to five times more common among
adolescentfemalesthanmales,onlyfemales wererecruited in
the larger study.
confidentiality agreements with the agencies, reviewed the
243 qualifying cases and summarized the files of the 201 fe-
males with open cases who had a history of maltreatment.
Two members of the research team and two clinical research-
ers independently adjudicated the summaries for eligibility
and to determine abuse exposures and severity. About half
(108/201) were ineligible, based on the following exclusion
stable environment (12%), and no confirmed abuse. An addi-
tional 6% could not be contacted. A letter describing the study
76 (82%) were enrolled in the larger study on the psychiatric
and physiological sequelae of maltreatment carried out overa
2-year period, with assessments every 6 months. Nine were
subsequentlyexcluded based oneligibility criteria. Of theeli-
gible youths, 38 (41%; M age ¼ 14.47, SD ¼ 1.00) female
youths participated in the present psychophysiological study.
We included 38 maltreated participants from the larger
sample of 67 maltreated females (see MacMillan et al.,
2009) for the following reasons: (a) of the 55/67 maltreated
participants who came to our laboratory for the psychophys-
iological portion of the study, an additional 15 (the oldest fe-
males of 55 total) participants were excluded from analysis
because they were too old and could not be aged matched
with the control females; and (b) the EEG data from 2 mal-
treated participants were not usable because of excessive ar-
tifact and/or technical malfunction.
was recruited from an existing database of children in the De-
partment of Psychology, Neuroscience & Behaviour at
McMaster University whose mothers had agreed at the
child’s birth to be contacted for future participation in re-
tory of pre- or postnatal problems. Controls were matched
with the maltreated sample, on a group level, with respect
to age, gender, handedness and zip code (a proxy for socio-
economic status [SES]). Controls had no history of involve-
ment with a CPA, and no maltreatment based on two self-re-
port measures: the Childhood Trauma Questionnaire (CTQ;
Bernstein & Fink, 1998) and the Childhood Experiences of
Violence Questionnaire (Walsh, MacMillan, Trocme, Jamie-
son, & Boyle, 2008). EEG data from one control participant
were excluded from analysis because of excessive artifact.
The control participants were a convenience sample and
tested in the laboratory on only one occasion. For a thorough
overview of thefull maltreatment and control samples used in
the present study, see MacMillan et al. (2009).
Consent to participate in the study for youths in the care of
the province was provided by the CPA; parental consent was
provided for those in the care of their parents. The present re-
search was approved by the Hamilton Health Sciences/
McMaster University Research Ethics Board. Participants re-
ceived $15 for each home assessment and $25 for each clinic
and laboratory visit.
Upon arrival to the laboratory, the procedures were explained
to the participants and written informed consent for the EEG
portion of the study was obtained. Participants had their rest-
ing EEG collected and then completed a batteryof self-report
personality questionnaires. All laboratory procedures were
conducted under the supervision of trained research staff.
EEG data collection.
EEG recording. Regional EEG was collected for 2 min
(1 min eyes open, 1 min eyes closed) using a Lycra stretch
cap (Electro-Cap International, Inc., Eaton, OH). Studies
have shown that EEG power estimates as short as 2 min have
proven reliable (Allen, Urry, Hitt, & Coan, 2004; Schmidt,
2008). The cap electrodes were positioned according to the
10/20 system of the International Federation (Jasper, 1958).
The experimenter used the blunt end of a Q-tip incombination
trode surface. Each electrode site was then filled with a small
amount of electrolyte gel that served as a conductor. Electrode
impedances below 10 kV per site and within 500 V between
homologous sites were considered acceptable.
EEGs were recorded from the left and right anterior, mid-
line, and posterior regions of the scalp (i.e., midfrontal: F3,
F4; central: C3, C4; parietal: P3, P3; occipital: O1, O2). All
active EEG sites were referenced to Cz during acquisition.
V. Miskovic et al.
A calibration signal (10 Hz/0.47 V rms sine wave) was in-
put through each amplifier prior to each data collection. The
output of this signal was 50 mV, with a gain of 10,000 (A/D
input range+2.5 V). The nine channels were amplified by
individual bioamplifiers (32-channel Custom SA Instrumen-
tation Bioamplifiers, San Diego, CA), with filter settings for
all channels set at 1 Hz (high pass) and 100 Hz (low pass).
The data from all nine channels were digitized on-line at a
sampling rate of 512 Hz.
EEG data reduction and quantification. The EEG data
were rereferenced to an average reference in software and
visually scanned for artifact because of movement (e.g., eye
blinks, body movements) and edited out using software devel-
oped by James Long Company (EEG Analysis Program, Ca-
roga Lake, NY).The EEG Analysis Program allowsthe opera-
tor toscroll through analog dataandadd/remove artifactmarks
with mouse and keyboard. Epochs marked as artifact are
marked for all channels and not used in subsequent analyses.
The electrode array used in the present study was extensive
enough to justify the use of an average reference (Marshall,
Bar-Haim, & Fox, 2002). Although average referencing may
lead to inflated EEG coherence values (Nunez et al., 1997),
it provides more accurate coherence estimates than the Cz ref-
(Fein, Raz, Brown, & Merrin, 1988).
Coherence was computed for the a-frequency band (7.5–
12.5 Hz) using the algorithm developed by Saltzberg, Burton,
Burch, Fletcher, and Michaels (1986). Measures of EEG co-
herence were derived for six intrahemispheric, left (F3–C3,
F3–P3, F3–O1, C3–P3, C3–O1, P3–O1) and right (F4–C4,
F4–P4, F4–O2, C4–P4, C4–O2, P4–O2), and four interhemi-
spheric (F3–F4, C3–C4, P3–P4, O1–O2) electrode pairs.
To ensure that there were no between-group differences in
the amount of EEG data removed because of artifacts, we
computed a ratio reflecting the number of discrete Fourier
transform windows included in the analyses, divided byepoch
duration length. There was no significant difference on this
EEG artifact ratio between the maltreated (M ¼ 1.38, SEM ¼
0.05) and control (M ¼ 1.33, SEM ¼ 0.10) groups (p ¼ .59).
Composite psychiatric measure
As part of the Youth Mood Project (see MacMillan et al.,
2009, for more information), a trained clinician administered
the Schedule for Affective Disorders and Schizophrenia for
School-Aged Children—Epidemiologic Version 5 (Orva-
schel, 1994) off site from the psychophysiology laboratory.
The schedule was administered at several time points. To cre-
ate a composite measure of overall psychiatric impairment,
we coded no symptoms present as 0, some symptoms present
as 1, and definitely present as 2 and then summed across the
following measures: current depression, dysthymic disorder,
mania, hypomania, cyclothymic disorder, separation anxiety
disorder, social phobia (including generalized subtype), spe-
cific phobia, panic disorder (with and without agoraphobia),
generalized anxiety disorder, PTSD, obsessive–compulsive
disorder, recurrent thoughts of death, suicidal ideation/plan/
attempt, substance abuse and dependence, alcohol abuse
and dependence, cigarette use, bulimia and anorexia nervosa,
and conduct and oppositional disorders. Symptoms that were
current at the time of the present study, as well as at two
separate assessment points (6 months later and 1 year later)
were pooled. The composite measure was standardized using
a Z-score transformation (range ¼ 4.48).
Childhood abuse and neglect measure
The CTQ (Bernstein & Fink, 1998) is a 28-item retrospective
self-report scale that assesses abuse and neglect occurring
during childhood or adolescence. The CTQ measures emo-
tional (“People in my family criticized me”), physical (“Peo-
ple in my family hit me so hard that it left bruises or marks”),
or tried to make me touch them”) and emotional (“My family
was a source of strength and support”) and physical (“I didn’t
have enough to eat”) neglect. Items are scored on a 5-point
Likert scale, ranging from never true to very often true. The
CTQ has strong psychometric properties (Bernstein & Fink,
1998; Bernstein et al., 1994).
Maltreatment was also indexed by the Childhood Experi-
ences of Violence Questionnaire (Walsh et al., 2008; We-
kerle, Miller, Wolfe, & Spindel, 2006). However, only data
from the CTQ are included in the present study, because we
required a continuous measure of maltreatment to test rela-
tions with EEG coherence.
To examine group differences on the sociodemographic and
participant characteristic variables, we performed indepen-
dent t tests (for continuous data) and chi-square analyses
(for categorical data).
Measures of EEG coherence between all intrahemispheric
pairs were averaged across the eyes-open and eyes-closed
resting conditions to form a composite index of left and right
intrahemispheric coherence. These grand mean measures
were normalized using the Fisher z transform (Fisher z ¼
0.5[ln(1 þ r) 2 ln(1 2 r)]). To examine group differences in
left and right hemispheric coherence, we performed a re-
peated-measures analysis of variance (ANOVA) using group
(controls, maltreated) asthe between-subjects factorand hemi-
sphere (left, right) as the within-subjects factor, on the trans-
formed coherence values. Differences in laterality were ex-
amined by computing the coherence laterality index on the
nontransformed composite coherence values using the for-
mula (laterality ¼ 100?(left – right)/[average(L þ R)]) as
described by Ito et al. (1998). A positive laterality score indi-
cates that left hemisphere coherence exceeds right hemi-
To determine the region(s) accounting for any possible
differences in intrahemispheric connectivity, we created re-
Atypical EEG coherence in child maltreatment
gion-specific coherence laterality indices. Regional coher-
ence measures were calculated using the Besthorn et al.
(1994) method for the spatial averaging of EEG coherence.
We performed a series of one-way ANOVAs on the coher-
ence laterality measures, using group (controls, maltreated)
as the between-subjects factor, separately for each region.
coherence, because they have previously been demonstrated
to positively correlate with the area of corresponding subre-
gions of the corpus callosum (Pogarell et al., 2005). We fo-
cused on the frontal (F3–F4) and occipital (O1–O2) elec-
trodes as the most salient poles of the anterior–posterior axis,
and combined the central and parietal electrodes into a com-
mon centroparietal site (C3–C4, P3–P4). These indices were
normalized using the Fisher z transform. We then computed a
repeated-measures ANOVA, using group (controls, mal-
treated) as the between-subjects factor and region (anterior,
posterior) as the within-subjects factor. Greenhouse–Geisser
corrected p values were applied where appropriate.
To examine the relations between child maltreatment,
atypical left hemisphere connectivity (left hemispheric EEG
coherence) and psychiatric impairment, we conducted a ser-
ies of linear regression analyses.
Sociodemographic and clinical data
Table 1 presents the sociodemographic and clinical data for
the control and maltreated groups. There were no significant
group differences in age at assessment (p . .05). However,
the maltreated group showed more pubertal development
than the control group, on indices of pubic hairand breast de-
group come from lower SES familiesthan females in the con-
trol group (p , .01). There were no between-group differ-
ences in the prevalence of current major depressive disorder
(p . .05) or PTSD (p . .05).
EEG coherence analyses
Intrahemispheric coherence. Therewas a significant Group?
Hemisphere interaction on a-band intrahemispheric coher-
ence, F (1, 60) ¼ 35.77, p ¼ .001. To decompose this inter-
action, we performed one-way ANOVAs with group as the
between-subjects factor on a-band intrahemispheric coher-
ence, separately for each hemisphere. As predicted, the mal-
treated group showed significantly higher left hemisphere co-
herence compared with the control group, F (1, 60) ¼ 58.59,
p ¼ .001 (see Figure 1). There were no significant group dif-
ferences for right hemisphere coherence (p . .05).
Across all scalp regions, the maltreated group (M ¼ 22.56,
SEM¼2.66)showed moreleftthanrighthemisphereEEG co-
herence than controls (M ¼ 22.23, SEM ¼ 2.42), as indicated
by a greater coherence laterality index F (1, 60) ¼ 33.55, p ¼
.001. Positive coherence laterality index scores indicate more
left than right hemisphere EEG coherence.
Regional coherence laterality. As predicted, the maltreated
group showed significantly greatercoherence laterality indices
91.08, p ¼ .001, and parietal, F (1, 60) ¼ 24.78, p ¼ .001,
regions than controls (see Figure 2). There was no significant
group difference for occipital coherence laterality (p . .05).
Interhemispheric coherence. There was a significant Group?
Region interaction on a-band interhemispheric coherence, F
(2, 59) ¼ 22.39, p ¼ .001. We performed one-way ANOVAs
using group as the between-subjects factor, separately for the
anterior, centroparietal, and posterior regions. As predicted,
the maltreated group (M ¼ 0.50, SE ¼ 0.03) compared with
the control group (M ¼ 0.69, SE ¼ 0.03) had lower anterior
interhemispheric EEG coherence, F (1, 60) ¼ 18.20, p ¼
.001. By contrast, the maltreated group (M ¼ 0.32, SE ¼
0.01) versus the control group (M ¼ 0.20, SE ¼ 0.02) had
higher centroparietal interhemispheric EEG coherence, F
in occipital coherence (p . .20).
EEG coherence analyses controlling
for confounding variables
We also conducted hierarchical regression analyses to exam-
ine if group differences in EEG coherence revealed by the
Table 1. Sociodemographic and clinical variables
for the control and maltreated groups
(n ¼ 38)
Sociodemographic and Individual Characteristics
Hollingshead Four Factor
Pubertal and Clinical Characteristics
Tanner breast development,
Stages 4 and 5 (%)
Tanner pubic hair, Stages
4 and 5 (%)
Current major depressive
Note: SES, socioeconomic status.
aData were missing from five maltreated participants.
V. Miskovic et al.
ANOVA analyses remained after controlling for the signifi-
cant group differences in pubertal status and SES. For each
equation, pubertal status and SES were entered in at Step 1
and group membership (1 ¼ maltreated, 2 ¼ control) was en-
tered in at Step 2. Group continued to be a significant pre-
dictor of left hemisphere EEG coherence (group b ¼ 20.79,
p ¼ .001), anterior interhemispheric EEG coherence (group
b ¼ 0.44, p ¼ .01), and centroparietal interhemispheric EEG
coherence (group b ¼ 20.51, p ¼ .001) and significantly im-
.05; see Table 2 for summaries).
Association of types of abuse and neglect
with brain activity
Associations between types of abuse and neglect and EEG
coherence measures were determined using a series of Pear-
son zero-order correlation coefficients. Table 3 summarizes
the results of these analyses. There was no association be-
tween right hemisphere coherence and childhood maltreat-
ment (ps . .05). However, left hemisphere coherence and
centroparietal interhemispheric coherence correlated posi-
tively with physical abuse and neglect.
Figure 1. Mean differences between the maltreated (n ¼ 38) and control (n ¼ 24) groups on average resting intrahemispheric a-band EEG co-
herenceshownseparatelyforthe leftandright cerebral hemispheres.Thecompositecoherencedatawere normalizedusingtheFisherztransform
prior to analysis. Bars represent standard errors.
Figure 2. Mean differences between the maltreated (n ¼ 38) and control (n ¼ 24) groups on regional EEG coherence laterality indices. Positive
coherence laterality indices indicate left hemisphere . right hemisphere coherence, and negative scores indicate right hemisphere . left hemi-
sphere coherence. Bars represent standard errors.
Atypical EEG coherence in child maltreatment
Modeling early adversity, left hemisphere development,
and psychiatric impairment
We next conducted a series of analyses to test whether left
hemisphere EEG coherence significantly predicted the score
of overall psychiatric impairment that was aggregated across
three separate assessment points. Furthermore, if left hemi-
sphere EEG coherence predicted psychiatric impairment,
we were interested in testing whether it mediated the effects
of maltreatment on this outcome. It is important to note that
the following analyses included only the maltreated sample.
According to the standard mediation model (Baron &
Kenny, 1986), mediation can be inferred when the following
criteria are met: (a) the independent variable predicts both the
putative mediatorand the dependent variable, (b) the putative
mediator predicts the dependent variable, and (c) the path
from the independent variable to the dependent variable is
made nonsignificant by the inclusion of the mediator into
the equation. Because the CTQ total score provides a contin-
uous measure of maltreatment, we used it as a predictoralong
with left hemisphere EEG coherence. We controlled for
group differences in pubertal development and SES. All pre-
dictors were centered prior to regression analyses, as recom-
mend by Aiken and West (1991).
We first regressed the dependent variable (psychiatric im-
pairment) and the putative mediator (left hemisphere EEG co-
herence) on the independent variable (child maltreatment, as
psychiatric impairment (b ¼ 0.33, p ¼ .03). High CTQ scores
also significantly predicted left hemisphere EEG coherence (b
lefthemisphere EEG coherence.Therewasadirect association
dicted increases in generalized psychiatric problems. Finally,
we regressed psychiatric impairment on both left hemisphere
EEG coherence and child maltreatment, resulting in a non-
atricimpairment (b ¼0.19, p¼.21),but asignificant associa-
tion with left hemisphere EEG coherence (b ¼ 0.38, p ¼ .02).
Accordingly, despite the relatively small sample size, our re-
sults suggest that excessive left hemisphere EEG coherence
mediated the effects of child maltreatment on the degree of
psychiatric impairment (see Figure 3).
This study demonstrated that child maltreatment was associ-
ated with atypical resting brain electrical activity in adoles-
cent females. We found that maltreated females showed
greater left hemisphere EEG coherence than their nonabused
gender- and age-matched peers. The maltreated group also
showed a reversal of the typical developmental pattern and
exhibited more overall left than right hemisphere EEG coher-
ence. Lateralized differences in EEG coherence were greatest
in the most anterior scalp regions. These results support the
preliminary report of aberrant cortical connectivity in abused
children (Ito et al., 1998) and extend the findings to a larger
sample of nonhospitalized adolescents.
mispheric EEG coherence between the maltreated and control
terhemispheric coherence compared to controls, but increased
centroparietal coherence. The severity of maltreatment (as in-
trahemispheric EEG coherence and centroparietal interhemi-
spheric EEG coherence. Of the different subtypes of abuse
and neglect, the strongest relation emerged between physical
neglect and EEG coherence. This finding is corroborated by
recent evidence concerning the adverse effects of neglect
on brain development and function in primates (Maestripieri
etal.,2006)aswellashuman children(Marshall et al.,2008).
Of importance, we found that excessive left hemisphere
EEG coherence mediated the effects of child maltreatment
even after controlling for significant group differences in pu-
bertal development and SES.
What do differences in left hemisphere EEG coherence
Similar to Ito and colleagues (1998), we interpret greater left
hemisphere coherence as reflecting decreased amounts of ce-
Table 2. Summary of hierarchical regression analyses
controlling for pubertal status and SES
Left Hemisphere Coherence
Anterior Interhemispheric Coherence
Centroparietal Interhemispheric Coherence
Note: SES, socioeconomic status.
*p ,.05. **p ,.01.
V. Miskovic et al.
rebral differentiation and development. There is some evi-
dence to suggest that decreased coherence is related to opti-
mal organization of cortical networks (Thatcher et al.,
2008). For instance, decreased EEG coherence predicts
higher intelligence and efficiency of cognitive processing
(Gasser, Verleger, Bacher, & Sroka, 1987; Silberstein et al.,
2004; Thatcher et al., 2005) and average connection density
decreases with a concomitant rise in brain size and complex-
ity (Ringo, 1991). Although we did not administer any cog-
nitive tasks, our results may explain some of the deficits on
by maltreated individuals (Navalta et al., 2006; Teicher et al.,
1997). Atypical circuitry of the left hemisphere may also ac-
count for some of the deficits and delays in language function
among maltreated children (Culp et al., 1991).
There is much room for ontogenetic sculpting of human
brain structure and function, especially in the first two de-
cades of postnatal life (e.g., Edelman, 1987). For example,
anatomical, neurochemical, and electrocortical evidence sug-
gests that the frontal lobes, in particular, continue to develop
into adolescence and young adulthood (Benes, 2001; Gasser
et al., 1988; Huttenlocher, 1999; Segalowitz & Davies,
2004). Species-typical caregiving experiences are important
for normal brain development. Child maltreatment represents
an extreme deviation from an average expectable caregiving
milieu and provides an inadequate environment for the estab-
lishment of normal brain structure and function.
It is not immediately obvious why maltreatment should be
associated with atypical circuitry of the left cerebral hemi-
such as axonal sprouting, synaptogenesis, synaptic pruning,
nate among these possibilities (Thatcher, 1992).
One possibility is that adverse experiences occurring dur-
ing periods of peak development are particularly likely to in-
terfere with normal neurobiological maturation. The left and
right cerebral hemispheres have unique EEG maturational
profiles, with cyclical changes in the relative rates and peak
periods of development across the first decade of postnatal
life (Thatcher, Walker, & Giudice, 1987). Accordingly,
some authors (e.g., Ito et al., 1998) have suggested that child
especially likely to affect the left hemisphere. Unfortunately,
age of maltreatment onset to be able to formally test this hy-
pothesis. However, it is interesting to note that a recent fMRI
study found left basal ganglia dysfunction in young adults
whowere maltreated (Dillon et al., 2009), suggesting that lat-
eralized effects are also present for subcortical structures,
which have different developmental sensitive periods.
ical caregiving experience on the function of monoaminergic
neurotransmitters (see also Dillon et al., 2009; Ito et al., 1998).
of maternal rejection show reduced levels of serotonin (5-hy-
droxyindoleacetic acid) and dopamine (homovanillic acid) me-
tabolites in their cerebrospinal fluid (Maestripieri et al., 2006). It
is interesting that these monoaminergic systems are lateralized in
Table 3. Pearson zero-order correlations among measures of EEG coherence and different subtypes of abuse
1. Intra. L-coherence
2. Intra. R-coherence
3. Ant. inter. coherence
4. Cnp. inter. coherence
5. Post. inter. coherence
6. CTQ emotional abuse
7. CTQ physical abuse
8. CTQ sexual abuse
10. CTQ physical neglect
11. CTQ total score
Note: Intra. L-coherence, intrahemispheric left hemisphere coherence; Intra. R-coherence, intrahemispheric right hemisphere coherence; Ant. inter. coherence,
anterior interhemispheric coherence; Cnp. inter. coherence, centroparietal interhemispheric coherence; Post. inter. coherence, posterior interhemispheric coher-
ence; CTQ, Childhood Trauma Questionnaire.
†p, .07. *p, .05. **p, .01.
Figure 3.Amodeltestingtherelationamongchildmaltreatment (asassessed
by the Childhood Trauma Questionnaire), left hemisphere EEG coherence,
and degree of psychiatric impairment (controlling for pubertal status and so-
cioeconomic status). The weights represent standardized regression coeffi-
ber indicates an indirect association.
Atypical EEG coherence in child maltreatment
the human brain (Arato et al., 1991) and implicated in brain de-
velopment (Sodhi & Sanders-Bush, 2004; Todd, 1992). For
example, serotonin metabolites are higher in the right than
the lefthumancerebral hemisphere (Aratoetal., 1991).Deple-
tion of serotonin, potentially induced by child maltreatment,
may therefore lead to impaired maturation of the left hemi-
sphere, which is not able to compensate for reduced serotonin
levels. This is an interesting, although speculative proposition,
which awaits future evidence from studies with maltreated hu-
man populations. It would be an obvious advantage to employ
more direct indices of neural function (e.g., measurement of
neurotransmitter metabolites) to better characterize the effects
of child maltreatment on brain structure and function.
What do differences in interhemispheric EEG coherence
Giventhepositivecorrelation between EEG interhemispheric
coherence and regional corpus callosum area (Pogarell et al.,
2005), as well as reports of reduced corpus callosum size in
abused children (De Bellis et al., 1999, 2002; Teicher et al.,
2004), our results may provide electrophysiological evidence
for anterior commissural fiber atrophy. However, our finding
of increased centroparietal interhemispheric coherence in the
maltreated group seems counterintuitive. There are a couple of
studies have reported that child maltreatment is linked to
smaller corpus callosum size particularly in males (De Bellis
et al., 1999; Teicher et al., 1997), suggesting the need to con-
sider potential sex effects when examining the influence of
early adversity on callosal development. Similarly, a study
examining the effect of prenatal stress on the development
of the primate corpus callosum (Coe, Lubach, & Schneider,
2002) suggests that there are both sex- and region-specific ef-
fects on the development of this brain structure. In particular,
this study found that prenatal adversity led to increases in the
posterior regions of the corpus callosum among females, but
decreases in corpus callosum size among males. Thus, it is
possible that there are complex interactions between sex
and region that were not capable of being addressed by our
study. Second, recent evidence (Davey, Victor, & Schiff,
2000) suggests that subcortical structures (thalamus, basal
ganglia) contribute to sculpting patterns of EEG coherence,
so that caution is urged in attributing any observed differ-
ences solely to corticocortical connections crossing the cor-
However, differences in interhemispheric EEG coherence
between the maltreated and control females generally corrob-
orate both the nonhuman animal (Berrebi et al., 1988; Denen-
berg, 1981; Juraska & Kopcik, 1988; Sanchez et al., 1998) and
human (De Bellis et al., 1999, 2002; Teicher et al., 2004) evi-
mised by childhood rearing experiences. Enhanced glucocorti-
coid circulation, associated with the stress of maltreatment,
may provide one potential mechanism linking early adversity
to impaired callosal development (Kaur, Wu, Wen, & Ling,
1994). Such developmental alterations may eventually influ-
ence patterns of functional lateralization, including the later-
alization of emotion and emotion regulatory systems (Misko-
vic, Schmidt, Georgiades, Boyle, & MacMillan, 2009).
Linking child maltreatment, the left hemisphere,
Our model has considered the links among early adversity,
left brain function, and general psychopathology. We found
preliminary evidence that atypical circuitry of the left hemi-
sphere mediated the effects of child maltreatment on subse-
quent psychiatric impairment. Our study is correlational in
However, one potential interpretation of our findings is that
connectivity deficits in the left hemisphere are associated
with a reduced ability to regulate emotions, and in particular,
negative emotions. The left frontal cortex has been suggested
to exert a main inhibitory influence over subcortical regions
such as the amygdala (Davidson, 2002; Davidson et al.,
2000). In support of this suggestion, an inverse relation be-
tween left anterior cortex and amygdala metabolism has
been reported in a previous positron emission tomography
study (Abercrombie et al., 1996), whereas greater left frontal
brain electrical activity predicts an attenuated startle response
following affective challenge (Jackson et al., 2003). Of im-
portance, the startle reflex is modulated by the amygdala.
Similarly, an fMRI study found evidence for the recruitment
of a left-lateralized neural circuit during the regulation of
negative affect (Oschner et al., 2002). Smaller left, relative
to right, orbitofrontal cortex volume has also been related to
increased impulsivity and aggression (Antonucci et al., 2006).
Most recently, Johnstone and colleagues (2007) have reported
left-lateralized brain activation during the downregulation of
negative affect among healthy, nondepressed participants. It
was interesting that nondepressed individuals showed an in-
cortex and the amygdala, during an emotion regulation task.
The results from that study also implicated a dysfunction of
the left-lateralized neural circuit during emotion regulation in
the pathophysiology of depression. Deviant cortical organiza-
tion ofthelefthemisphere, associatedwithchild maltreatment,
may make these adolescents more vulnerable to subsequent
stress and more likely to experience psychiatric symptoms.
One other parsimonious interpretation of our findings isthat
child maltreatment is associated with a depletion of the brain’s
differentially lateralized monoaminergic systems (e.g., seroto-
nin). Subsequently, monoaminergic depletion may be a com-
mon factor that accounts for (a) a maturational lag of the left
hemisphere (as a consequence, of the monoamines’ neuro-
trophic effects) as well as (b) difficulties in successful emotion
regulation, leading to increased susceptibility to psychiatric
symptoms. It is important to note that serotonin function (espe-
cially serotonin depletion) has long been linked to behavioral
impulsivity in nonhuman animal models (e.g., Brunner &
Hen, 1997). However, until there is more evidence, we urge
V. Miskovic et al.
caution in interpreting this model and onlysuggest it as atenta-
tive explanation for our findings.
At least another possible alternative model is that abusive
parenting may be genetically cosegregated with atypical left
hemisphere function and psychiatric problems (e.g., Green,
Voeller, Gaines, & Kubie, 1981). Similar issues have been
exists concerning the role of hippocampal volume, either as a
risk factor for PTSD ora consequence of traumatic experience
(Gilbertson et al., 2002).
one or more variables. Outcomes such as emotion regulatory
problems and psychopathological risk are almost certainly
determined by cumulative risk factors, originating at multi-
ple, reciprocally interacting biopsychosocial levels (Samer-
off, 2000). Such nonlinear processes are among the core te-
nets of developmental psychopathology (Rutter & Sroufe,
2000; Sroufe & Rutter, 1984).
to tease apart potential sex-specific effects of maltreatment on
brain function (Teicher et al., 2003), because we had an exclu-
sively female sample. Second, we used measures of scalp EEG
coherence to make inferences about functional connectivity.
Scalp coherence can produce spurious coherence values as a re-
sult of volume conduction. Accordingly, future studies should
use dense-array electrophysiology to allow for the computation
of source coherence, thereby providing more accurate measures
of corticocortical coupling (Hoechstetter et al., 2004). Third,
even though the adolescents were under CPA services, the reli-
ance on retrospective self-report measures to define child mal-
treatment, rather than more objective methods such as court re-
ports, was a limitation; however, these are also prone to bias.
the maltreatment had begun. Because development is time de-
pendent, early occurring insults are likely to lead to more dys-
tant to characterize the timing and nature of sensitive periods in
human socioemotional development, because this knowledge
may eventually translate into better intervention efforts. Some
it will be important to assess the stability of the neurobiological
dynamic, short-term changes, or more long-lasting alterations.
We have recently attempted to address some of these issues in
our laboratory (e.g., Miskovic et al., 2009).
sample size of maltreated adolescents. Issues of restricted
sample size pose a statistical challenge, given the importance
of large sample sizes for conducting reliable mediation anal-
yses (MacKinnon, Fairchild, & Fritz, 2007). However, such
concerns are offset when considered in the context of the dif-
ficulty involved in conducting research with highly vulnera-
ble populations and the potential theoretical and practical im-
portance of such work.
maltreatment can leave a lasting impact on resting brain func-
tion. Specifically, child maltreatment appears to be associated
with deficient left hemispheric development and disturbed in-
terhemispheric connectivity. Deficits in the circuitry of the
left hemisphere may mediate the effects of child maltreatment
on future psychiatric impairment. To be more precise, it is dif-
ficult to disambiguate whether the adverse effects on central
nervous system development are due to the experience of mal-
treatmentitself or the environmental stressorsthat are typically
thology). It should be noted that we attempted to control for
some of these confounding factors. Studies of siblings discor-
dant for childhood maltreatment and preclinical models can be
with cerebral development and behavioral organization.
One of the implications of this study isthat the use of non-
invasive psychophysiological measures in developmental
populations can index the middle level of analysis (Segalowitz
& Schmidt, 2008) that helps to link experience, brain, and
psychopathology. Establishing such links is crucial for gain-
ing insight into complex developmental processes, especially
iors (normal or abnormal) but the brain systems that are in-
volved in producing such behaviors (Knudsen, 2004).
Finally, it is important to note that although we have pro-
posed a putative pathway linking left hemispheric aberrations
to atypical cerebral development are less clear. Although we
have suggested several hypotheses (e.g., monoaminergic de-
ture research. Ultimately, such research will help us to identify
the biological processes that mediate or moderate the relations
between early adversity and future psychopathology.
Abercrombie, H. C., Schaefer, S. M., Larson, C. L., Ward, R. T., Holden, J.
F., Turski, P. A., et al. (1996). Medial prefrontal and amygdala glucose
metabolism in depressed and control subjects: An FDG-PET study. Psy-
chophysiology, 33, s17.
Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and inter-
preting interactions. Thousand Oaks, CA: Sage.
Allen,J. J.,Urry,H.L.,Hitt,S.K.,& Coan,J.A.(2004).Thestabilityofrest-
ing frontal electroencephalographic asymmetry in depression. Psycho-
physiology, 41, 269–280.
Antonucci, A. S., Gansler, D. A., Tan, S., Bhadelia, R., Patz, S., & Fulwiler,
C. (2006). Orbitofrontal correlates of aggression and impulsivity in psy-
chiatric patients. Psychiatry Research: Neuroimaging, 147, 213–220.
Atypical EEG coherence in child maltreatment
Arato, M., Frecska, E., Maccrimmon, D. J., Guscott, R., Saxena, B., Tekes,
K., et al. (1991). Serotonergic interhemispheric asymmetry: Neurochem-
ical and pharmaco-EEG evidence. Progress in Neuro-Psychopharmacol-
ogy and Biological Psychiatry, 15, 759–764.
Baron, R. M., & Kenny, D. A. (1986). The moderator–mediator variable dis-
tical considerations. Journal of Personality and Social Psychology, 51,
Bell, M. A., & Fox, N. A. (1996). Crawling experience is related to changes
in cortical organization during infancy: Evidence from EEG coherence.
Developmental Psychobiology, 29, 551–561.
neurotransmitter systems and their interactions. In C. Nelson & M. Luci-
ana (Eds.), Handbook of developmental cognitive neuroscience (pp. 79–
92). Cambridge, MA: MIT Press.
spective self-report manual. San Antonio, TX: Psychological Corporation.
Bernstein, D. P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., Wenzel,
sure of child abuse and neglect. American Journal of Psychiatry, 151,
Berrebi, A. S., Fitch, R. H., Ralphe, D. L., Denenberg, J. O., Friedrich, V. L.,
of sex, early experience and age. Brain Research, 438, 216–224.
Besthorn, C., Forstl, H., Geiger-Kabisch, C., Sattel, H., Gasser, T., & Schrei-
ter-Gasser, U. (1994). EEG coherence in Alzheimer disease. Electroen-
cephalography and Clinical Neurophysiology, 90, 242–245.
Bremner, J. D., Randall, P., Vermetten, E., Staib, L., Bronen, R. A., Mazure,
pocampal volume in posttraumatic stress disorder related to childhood
physical and sexual abuse—A preliminary report. Biological Psychiatry,
Brunner, D., & Hen, R. (1997). Insights into the neurobiology of impulsive
behavior from serotonin receptor knockout mice. Annals of the New York
Academy of Sciences, 836, 81–105.
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory struc-
tures of the mind. Development and Psychopathology, 6, 533–549.
Cicchetti, D., & Valentino, K. (2006). An ecological-transactional perspec-
and its influence on child development. In D. Cicchetti & D. J. Cohen
(Eds.), Developmental Psychopathology: Vol. 3. Risk, disorder and
adaptation (2nd ed., pp. 129–201). Hoboken, NJ: Wiley.
Coben, R., Clarke, A., Hudspeth, W., & Barry, R. (2008). EEG power and
coherence in autistic spectrum disorder. Clinical Neurophysiology, 119,
Coe, C. L., Lubach, G. R., & Schneider, M. L. (2002). Prenatal disturbance
alters the size of the corpus callosum in young monkeys. Developmental
Psychobiology, 41, 178–185.
(1991). Maltreated children’s language and speech development: Abused,
neglected and abused and neglected. First Language, 11, 377–389.
Curtis, W. J., & Cicchetti, D. (2007). Emotion and resilience: A multilevel
investigation of hemispheric electroencephalogram asymmetry and emo-
tion regulation in maltreated and nonmaltreated children. Development
and Psychopathology, 19, 811–840.
d’Alfonso, A. A. L., van Honk, J., Hermans, E., Postma, A., & de Haan,
E. H. F. (2000). Laterality effects in selective attention to threat after
repetitive transcranial magnetic stimulation at the prefrontal cortex in
female subjects. Neuroscience Letters, 280, 195–198.
Danese, A., Pariante, C. M., Caspi, A., Taylor, A., & Poulton, R. (2007).
Childhood maltreatment predicts adult inflammation in a life-course
study. Proceedings of the National Academy of Sciences of the United
States of America, 104, 1319–1324.
Davey, M. P., Victor, J. D., & Schiff, N. D. (2000). Power spectra and coher-
ence in the EEG of a vegetative patient with severe asymmetric brain
damage. Clinical Neurophysiology, 111, 1949–1954.
Davidson, R. J. (2002). Anxietyand affective style: Role of prefrontal cortex
and amygdala. Biological Psychiatry, 51, 68–80.
Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000). Emotion, plasticity,
context, and regulation: Perspectives from affective neuroscience. Psy-
chological Bulletin, 126, 890–909.
development of maltreated children and its implications for research,
treatment, and policy. Development and Psychopathology, 13, 539–564.
De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N.,
Boring, A. M., et al. (1999). Bennett Research Award. Developmental
traumatology. Part II: Brain development. Biological Psychiatry, 45,
De Bellis, M. D., Keshavan, M. S., Shifflett, H., Iyengar, S., Beers, S. R.,
Hall, J., et al. (2002). Brain structures in pediatric maltreatment-related
ological Psychiatry, 52, 1066–1078.
Denenberg, V. H. (1981). Hemispheric laterality in animalsand the effects of
early experience. Behavioral Brain Science, 4, 1–49.
Dillon, D. G., Holmes, A. J., Birk, J. L., Brooks, N., Lyons-Ruth, K., & Piz-
zagalli, D. A. (2009). Childhood adversity is associated with left basal
ganglia dysfunction during reward anticipation in adulthood. Biological
Psychiatry, 66, 206–213.
Edelman, G. M. (1987). Neural Darwinism: The theory of neuronal group
selection. New York: Basic Books.
Fein, G., Raz, J., Brown, F. F., & Merrin, E. L. (1988). Common reference
coherence data are confounded by power and phase effects. Electroen-
cephalography and Clinical Neurophysiology, 69, 581–584.
Felitti, V., Anda, R., Nordernberg, D., Williamson, D., Spitz, A., Edwards,
V., et al. (1998). Relationship of childhood abuse to many of the leading
causes of death in adults: The adverse childhood experiences (ACE)
study. American Journal of Preventative Medicine, 14, 245–258.
development: Relations to cognitive and affective behavior over the first
year of life. Annals of the New York Academyof Sciences, 608, 677–704.
Gasser, T., Jennen-Steinmetz, C., & Verleger, R. (1987). EEG coherence at
rest and during a visual task in two groups of children. Electroencepha-
lography and Clinical Neurophysiology, 67, 151–158.
Gasser, T., Verleger, R., Bacher, P., & Sroka, I. (1988). Development of the
EEG of school age children and adolescents. II. Topography. Electroen-
cephalography and Clinical Neurophysiology, 69, 91–99.
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B.,
Orr, S. P., et al. (2002). Smaller hippocampal volume predicts pathologic
vulnerability to psychological trauma. Nature Neuroscience, 5, 1242–
Green, A., Voeller, K., Gaines, R., & Kubie, J. (1981). Neurological impair-
ment in maltreated children. Child Abuse & Neglect, 5, 129–134.
Gur, R. C., Packer, I. K., Hungerbuhler, J. P., Reivich, M., Obrist, W. D.,
Amarnek, W. S., et al. (1980). Differences in the distribution of gray and
white matter in human cerebral hemispheres. Science, 207, 1226–1228.
Harlow, H. F., Dodsworth, R. O., & Harlow, M. K. (1965). Total social iso-
lation in monkeys. Proceedings of the National Academy of Sciences of
the United States of America, 54, 90–97.
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R.,
et al. (2000). Pituitary-adrenal and autonomic responsesto stress in wo-
men after sexual and physical abuse in childhood. Journal of the Amer-
ican Medical Association, 284, 592–597.
Hoechstetter, K., Bornfleth, H., Weckesser, D., Ille, N., Berg, P., & Scherg,
M. (2004). BESA source coherence: A new method to study cortical os-
cillatory coupling. Brain Topography, 16, 233–238.
chology, 16, 347–349.
dence for aberrant cortical development in abused children: A quantita-
tive EEG study. Journal of Neuropsychiatry & Clinical Neurosciences,
Ito, Y., Teicher, M. H., Glod, C. A., Harper, D., Magnus, E., & Gelbard, H.
A. (1993). Increased prevalence of electrophysiological abnormalities in
children with psychological, physical, and sexual abuse. Journal of Neu-
ropsychiatry & Clinical Neurosciences, 5, 401–408.
Jackson, D. C., Mueller, C. J., Dolski, L., Dalton, K. M., Nitschke, J. B., &
Urry, H. L. (2003). Now you feel it, now you don’t: Frontal brain electri-
cal asymmetry and individual differences in emotion regulation. Psycho-
logical Science, 14, 612–617.
Jasper, H. H. (1958). The ten-twenty electrode system of the International
Federation. Electroencephalography and Clinical Neurophysiology, 10,
Johnson, J. G., Cohen, P., Brown, J., Smailes, E. M., & Bernstein, D. P.
(1999). Childhood maltreatment increases risk for personality disorders
during early adulthood. Archives of General Psychiatry, 56, 600–606.
Johnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., & Davidson, R.
J. (2007).Failure to regulate:Counterproductive recruitmentof top-down
V. Miskovic et al.
prefrontal-subcortical circuitry in major depression. Journal of Neuro-
science, 27, 8877–8884.
Kaur, C., Wu, C., Wen, C. Y., & Ling, E. A. (1994). The effects of subcuta-
neous injections of glucocorticoids on amoeboid microglia in postnatal
rats. Archives of Histology and Cytology, 57, 449–459.
Kessler,R. C., McGonagle,K. A.,Zhao, S., Nelson,C. B., Hughes, M., Esh-
leman, S., et al. (1994). Lifetime and 12-monthprevalence of DSM-III-R
psychiatric disorders in the United States: results from the national co-
morbidity survey. Archives of General Psychiatry, 51, 8–19.
and the evidence. In N. A. Fox & R. J. Davidson (Eds.), The psychobiol-
ogy of affective development (pp. 259–292). Hillsdale, NJ: Erlbaum.
Knudsen, E. I. (2004). Sensitive periods in the development of the brain and
behavior. Journal of Cognitive Neuroscience, 16, 1412–1425.
Lewis, D. O. (1992). From abuse to violence: Psychophysiological conse-
quences of maltreatment. Journal of the American Academy of Child &
Adolescent Psychiatry, 31, 383–391.
Annual Review of Psychology, 58, 593–614.
MacMillan,H.L.,Fleming,J.E.,Streiner,D. L., Lin, E.,Boyle,M.H., Jamie-
son, E., et al. (2001). Childhood abuse and lifetime psychopathology in a
community sample. American Journal of Psychiatry, 158, 1878–1883.
MacMillan, H. L., Georgiades, K., Duku, E. K., Shea, A., Steiner, M., Niec,
A., et al. (2009). Cortisol responses to stress in female youths exposed to
childhood maltreatment: Results of the Youth Mood Project. Biological
Psychiatry, 66, 62–68.
Maestripieri, D., Higley, J. D., Lindell, S. G., Newman, T. K., McCormack,
K. M., & Sanchez, M. M. (2006). Early maternal rejection affects the
development of monoaminergic systems and adult abusive parenting in
rhesus macaques (Macaca mulatta). Behavioral Neuroscience, 120,
Manly, J. T., Kim, J. E., Rogosch, F. A., & Cicchetti, D. (2001). Dimensions
of child maltreatment and children’s adjustment: Contributions of devel-
opmental timing and subtype. Development and Psychopathology, 13,
Marshall, P. J., Bar-Haim, Y., & Fox, N. A. (2002). Development of the EEG
Marshall, P. J., Reeb, B. C., Fox, N. A., Nelson, C. A., & Zeanah, C. H.
(2008).Effectsof early interventionon EEG powerand coherence in pre-
viously institutionalized children in Romania. Development and Psycho-
pathology, 20, 861–880.
Miskovic, V., Schmidt, L. A., Boyle, M. H., & Saigal, S. (2009). Regional
electroencephalogram (EEG) spectral power and hemispheric coherence
in young adults born at extremely low birth weight. Clinical Neurophys-
iology, 120, 231–238.
Miskovic, V., Schmidt, L. A., Georgiades, K., Boyle, M., & MacMillan, H.
L. (2009). Stability of resting frontal electroencephalogram (EEG) asym-
metryand cardiac vagal tone in adolescent females exposed to child mal-
treatment. Developmental Psychobiology, 51, 474–487.
Mullen, P. E., Martin, J. C., Romans, S. E., & Herbison, G. P. (1996). The
long-term impact of the physical, emotional, and sexual abuse of chil-
dren: A community study. Child Abuse & Neglect, 20, 7–21.
Murias, M., Swanson, J. M., & Srinivasan, R. (2006). Functional connectiv-
ity of frontal cortex in healthy and ADHD children reflected in EEG co-
herence. Cerebral Cortex, 17, 1788–1799.
(2006). Effects of childhood sexual abuse on neuropsychological and
cognitive function in college women. Journal of Neuropsychiatry &
Clinical Neurosciences, 18, 45–53.
Neumann, D. A., Houskamp, B. M., Pollack, V. E., & Briere, J. (1996). The
review. Child Maltreatment, 1, 6–16.
Nunez, P. L. (1981). Electrical fields of the brain: The neurophysics of EEG.
New York: Oxford University Press.
Nunez, P. L., Srinivasan, R., Westdorp, A. F., Wijesinghe, R. S., Tucker, D.
M.,Silberstein, R.B.et al.(1997).EEGcoherency.I: Statistics,reference
tation at multiple scales. Electroencephalography and Clinical Neuro-
physiology, 103, 499–515.
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Re-
thinking feelings: An fMRI study of the cognitive regulation of emotion.
Journal of Cognitive Neuroscience, 14, 1215–1229.
Orvaschel, H. (1994). Schedule for Affective Disorders and Schizophrenia
for School-Aged Children—Epidemiologic version 5 (K-SADS-E). Fort
Lauderdale, FL: Nova Southeastern University.
(2005). EEG coherence reflects regional corpus callosum area in Alz-
heimer’s disease. Journal of Neurology, Neurosurgery & Psychiatry,
Pollak, S. D. (2005). Early adversity and mechanisms of plasticity: Integrat-
ing affective neuroscience with developmental approaches to psychopa-
thology. Development and Psychopathology, 17, 735–752
brain event-related potentials and emotion processing in maltreated chil-
dren. Child Development, 68, 773–787.
Ringo, J. L. (1991). Neuronal interconnection as a function of brain size.
Brain Behavior and Evolution, 38, 1–6.
Rogosch, F. A., & Cicchetti, D. (2004). Child maltreatment and emergent
personality organization: Perspectives from the five-factor model. Jour-
nal of Abnormal Child Psychology, 32, 123–145.
Rogosch, F. A., & Cicchetti, D. (2005). Child maltreatment, attention net-
works,and potentialprecursorsto borderlinepersonalitydisorder.Devel-
opment and Psychopathology, 17, 1071–1089.
Rutter, M., & Sroufe, A. L. (2000). Developmental psychopathology: Con-
cepts and challenges. Development and Psychopathology, 12, 265–296.
Saltzberg, B., Burton, D. B., Burch, N. R., Fletcher, J., & Michaels, R.
(1986). Electrophysiological measures of regional neural interactive cou-
pling: Linear and non-linear dependence relationships among multiple
channel electroencephalographic recordings. International Journal of
Biomedical Computing, 18, 77–87.
opment and Psychopathology, 12, 297–312.
Sanchez, M. M., Hearn, E. F., Dung, D., Rilling, J. K., & Herndon, J. G.
(1998). Differential rearing affects corpus callosum size and cognitive
function of rhesus monkeys. Brain Research, 812, 38–49.
Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse expe-
from rodent and primate models.Development and Psychopathology, 13,
Schiffer, F., Teicher, M. H., & Papanicolaou, A. C. (1995). Evoked potential
evidence for right brain activity during recall of traumatic memories.
Journal of Neuropsychiatry & Clinical Neurosciences, 7, 169–175.
Schmidt, L. A. (2008). Patterns of second-by-second resting frontal brain
(EEG) asymmetry and their relation to heart rate and temperament in 9-
month-old human infants. Personality & Individual Differences, 44,
Schutter, D. J. L. G., van Honk, J., d’Alfonso, A. A. L., Postma, A., & de
Haan, E. H. F. (2001). Effects of slow rTMS at the right dorsolateral pre-
frontal cortex on EEG asymmetryand mood. NeuroReport, 12, 445–447.
lobe: An electrophysiological strategy. Brain and Cognition, 55, 116–133.
Segalowitz, S. J., & Schmidt, L. A. (2008). Capturing the dynamic endophe-
& S. J. Segalowitz (Eds.), Developmental psychophysiology: Theory, sys-
tems and methods (pp. 1–12). New York: Cambridge University Press.
Silberstein, R. B., Song, J., Nunez,P. L. & Park, W. (2004). Dynamic sculpt-
Topography, 16, 249–254.
Sodhi, M. S., & Sanders-Bush, E. (2004). Serotonin and brain development.
International Review of Neurobiology, 59, 111–174.
Sroufe, L. A., & Rutter, M. (1984). The domain of developmental psychopa-
thology. Child Development, 55, 17–29.
Stein, M. B. (1997). Hippocampal volume in women victimized by child-
hood sexual abuse. Psychological Medicine, 27, 951–959.
C. M. (2006). Differential relationships of childhood abuse and neglect
subtypes to PTSD symptom clusters among adolescent inpatients. Jour-
nal of Traumatic Stress, 19, 229–239.
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the devel-
oping HPA axis. Hormones and Behavior, 50, 632–639.
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., &
Kim, D. M. (2003). The neurobiological consequences of early stress and
Teicher, M. H., Dumont, N. L., Ito, Y., Vaituzis, C., Giedd, J. N., & Ander-
sen, S. L. (2004). Childhood neglect is associated with reduced corpus
callosum area. Biological Psychiatry, 56, 80–85.
Atypical EEG coherence in child maltreatment
Teicher, M. H., Glod, C. A., Surrey, J., Swett, C. Jr. (1993). Early childhood
abuse and limbic system ratings in adult psychiatric outpatients. Journal
of Neuropsychiatry & Clinical Neurosciences, 5, 301–306.
Teicher, M. H., Ito, Y., Glod, C. A., Andersen, S. L., Dumont, N., & Acker-
man, E. (1997). Preliminaryevidence for abnormal cortical development
in physically and sexually abused children using EEG coherence and
MRI. Annals of the New York Academy of Sciences, 821, 160–175.
Thatcher, R. W. (1992). Cyclic cortical reorganization during early child-
hood. Brain and Cognition, 20, 24–50.
Thatcher, R. W., Krause, P. J., & Hrybyk, M. (1986). Cortico-cortical asso-
ciations and EEG coherence: A two-compartment model. Electroen-
cephalography and Clinical Neurophysiology, 64, 123–143.
Thatcher, R. W., McAlaster, R., Lester, M. L., Horst, R. L., & Cantor, D. S.
(1983). Hemispheric EEG asymmetries related to cognitive functioning
in children. In A. Perecuman (Ed.), Cognitive processing in the right
hemisphere. New York: Academic Press.
Thatcher, R. W., North, D., & Biver, C. (2005). EEG and intelligence: Uni-
variate and multivariate comparisons between EEG coherence, EEG
phase delay and power. Clinical Neurophysiology, 116, 2129–2141.
connections as measured by EEG coherence and phase delays. Human
Brain Mapping, 29, 1400–1415.
Thatcher, R. W., Walker, R. A., & Giudice, S. (1987). Human cerebral hemi-
spheres develop at different rates and ages. Science, 236, 1110–1113.
Todd, R. D. (1992). Neural development is regulated by classical neurotrans-
mitters: Dopamine D2 receptor stimulation enhances neurite outgrowth.
Biological Psychiatry, 31, 794–807.
Tucker, D. M., Roth, D. L., & Bair, T. B. (1986). Functional connections
among corticalregions:Topographyof EEG coherence. Electroencepha-
lography and Clinical Neurophysiology, 63, 242–250.
van der Kolk, B. A. (2003). The neurobiologyof childhood trauma and abuse.
Child and Adolescent Psychiatric Clinics of North America, 12, 293–317.
van der Kolk, B. A.,& Fisler,R. E. (1994). Childhood abuse and neglect and
loss of self-regulation. Bulletin of the Menninger Clinic, 58, 145–168.
Haan,E. H.F. (2002).1 HzrTMSover therightprefrontalcortex reduces
vigilant attentionto unmasked butnot to maskedfearful faces.Biological
Psychiatry, 52, 312–317.
Wada, Y., Nanbu, Y., Kikuchi, M., Koshino, Y., & Hashimoto, T. (1998).
Aberrant functional organization in schizophrenia: Analysis of EEG co-
herence during rest and photic stimulation in drug-naive patients. Neu-
ropsychobiology, 38, 63–69.
Walsh, C. A., MacMillan, H. L., Trocme, N., Jamieson, E., & Boyle, M. H.
(2008). Measurement of victimization in adolescence: Development and
validation of the Childhood Experiences of Violence Questionnaire.
Child Abuse & Neglect, 32, 1037–1057.
Wekerle, C., Miller, A. L., Wolfe, D. A., & Spindel, C. (2006). Child mal-
treatment. Toronto: Hogrefe & Huber.
Widom, C. S. (1989). The cycle of violence. Science, 244, 160–165.
Wismer Fries, A. B., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D.
(2005). Early experience in humans is associated with changes in neuro-
peptides critical for regulating social behavior. Proceedings of the Na-
tional Academy of Sciences of the United States Of America, 102,
V. Miskovic et al.