Hayashi et al. Journal of Physiological Anthropology (2018) 37:8
https://doi.org/10.1186/s40101-018-0167-9

ORIGINAL ARTICLE

Open Access

Enhanced Nogo-P3 amplitudes of mothers
compared with non-mother women during
an emotional Go/Nogo task
Sayuri Hayashi1* , Hiroko Wada1, Sung-Phil Kim2, Yuki Motomura3, Shigekazu Higuchi3 and Yeon-Kyu Kim3

Abstract
Background: It is known that emotion regulatory responses of humans are changed by the experiences they have,but in particular, they are changed by becoming a mother. A recent study has found how a woman’s emotion
regulatory response to a child’s crying changes after becoming a mother. However, mothers’ emotion regulatory
responses other than those to children and the association between emotion regulatory response and parental
stress are still unknown.
Methods: Eighteen healthy Japanese females (nine mothers and nine non-mothers) participated in the experiment.
They performed an emotional Go/Nogo task, with facial expressions of others (angry, happy, and neutral faces) usedas emotional stimuli. The percentage of correct responses, response time, and event-related potentials (ERPs) during
the task was measured.
Results: This comparison revealed that the mother group had a larger P3 (Nogo-P3) amplitude than the non-mothergroup when Nogo trials were held. This indicates that in mothers, there was greater activation of the behavioral
inhibition-related brain areas than in non-mother women when they inhibited inappropriate behavior following
recognition of facial expressions of others. In addition, in the mother group, there was a negative correlation between
parental stress levels and Nogo-P3 amplitudes evoked by angry faces. This suggests that there is a relation between
the level of parental stress of mothers and their emotion regulatory responses to angry faces.
Conclusions: Our results demonstrate that mothers’ emotion regulatory processes may differ from those of non-mothers
in response, not only to a child’s crying but also to expressions of emotions by others, and also suggest that the inhibitory
recognition activity of mothers can be affected by parental stress.
Keywords: Emotion regulation, Mothers, Parental stress, Behavioral inhibition, Event-related potentials (ERPs), Nogo-P3

Background
Emotion regulation, which is defined as the processes tocontrol one’s experience and expression of emotion, isessential for humans to lead a social life. Recent studies
suggest that it can be specifically changed by becoming amother. These studies also describe the importance ofemotion regulation to inhibit over-reactivity to children’s
crying, which would be related to mental health ofmothers [1–3].

* Correspondence: hayashi.sayuri.179@s.kyushu-u.ac.jp
1
Department of Kansei Science, Graduate School of Integrated Frontier
Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581,
Japan
Full list of author information is available at the end of the article

Mentally and physically healthy mothers and nonmother women have different patterns of brain activity
when they recognize negative emotion of children. Sucha difference between mothers and non-mother women isobserved in brain regions including the amygdala, insular cortex, anterior cingulate cortex, and ventral prefrontal cortex, and these areas related to regulating
cognitive and emotional processes [4]. Other studies describe that the brain activities of mothers including brain
regions related to emotion regulation are enhanced bynegative emotion of own children [5, 6]. The abovementioned change in patterns of brain activity is considered
to reflect the change in emotion regulation that resultsfrom becoming a mother. It has been also reported that

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Hayashi et al. Journal of Physiological Anthropology (2018) 37:8

the activity of the right lateral frontal pole and rightinferior frontal gyrus in the prefrontal cortex is greaterin mothers who display a high level of sensitivity to children than in mothers with a low sensitivity when they
hear children crying [7]. In addition, it is suggested thatthe prefrontal cortex activation, especially in the left side[8], reflects ability to regulate an initial negative response
to infant cries, making possible a more sensitive response to the infant [2]. Since these regions are associated with emotion regulation [9, 10], integration of
information, and judgments to realize a goal [11], thelevel of sensitivity of mothers of infants is considered to
be associated with activation of the brain function that
affects the mothers’ emotion regulation, especially behavioral inhibition, when they see their children crying.
It is considered that such characteristics of emotion
regulation-related brain function of mothers are formed
because emotion regulation (and the associated behavior) required for the period when women are the motherof an infant is different from that required for otherperiods of life [1, 2].
However, little is known about the brain activity associated with emotion regulation of mothers when theyobserve general emotional stimuli (other persons’ facial
expressions, scenic images, etc.) other than a child’s cry.
Given the fact that emotion regulation plays a crucialrole in enabling humans to lead a social life, emotion
regulation of mothers in situations often encountered ina general social life needs to be investigated. In addition,a correlation between emotion regulation and the levelof parental stress, which is suggested to be associatedwith decreased sensitivity to children and inappropriate
responses to infant behavior (e.g., abuse) [3], has notbeen clarified yet. In this study, therefore, we investigated emotion regulation of mothers when they recognized other persons’ facial expressions. Since previous
studies have consistently found brain activity related tobehavioral inhibition during emotion regulation, thisstudy focused on such behavioral inhibition-related brain
activity, particularly at the time of recognition of emotional stimuli. We also investigated a correlation between the level of parental stress and such brain activity.
For the evaluation of behavioral inhibition-related
brain activity elicited by the recognition of emotional
stimuli, we measured event-related potentials (ERPs)
when subjects performed a Go/Nogo task using emotional stimuli. During a Go/Nogo task, Go trials that require subjects to execute a response and Nogo trials
requiring them to withhold a response are presented. It
is known that Nogo trials evoke two ERP components
reflecting behavioral inhibition-related brain processing
where each component reflects a different processing
stage. The first component is called Nogo-N2, which is anegative component generated mainly in the frontal

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region about 200–400 ms after stimulus presentation.
Nogo-N2 reportedly reflects one’s monitoring of competing choices and struggling to decide between the
choices [12, 13]. The second component is called NogoP3, which is a positive component generated in thefronto-central region about 400–600 ms after stimulus
presentation. Nogo-P3 is known to reflect brain processing associated with cognitive and behavioral inhibition[14]. When emotional stimuli are used as the stimulus
presented in the Go/Nogo task, the influence of subjects’
emotion regulation is reflected in these ERP components. For example, it has been reported that highly impulsive individuals had larger Nogo-P3 amplitudes thanless-impulsive individuals only when stimuli with a highemotional valence were presented as the Nogo stimulus[15]. Furthermore, in this study, we also examined a correlation between parental stress of mothers and their
ERPs when performing the Go/Nogo task, to investigate
the influence of parental stress on emotion regulation.
Parental stress of mothers can be measured with a questionnaire called the Parental Stress Index (PSI) form, andthe total PSI score obtained from the questionnaire canindicate the level of overall parental stress of mothers ofinfants [16].
Based on the considerations above, we draw the following two hypotheses to be addressed:a) If mothers of infants have more activity in brain
areas related to emotion regulation, especially behavioral
inhibition, even when general emotional stimuli are presented, the Nogo-2 and Nogo-P3 of mothers shouldhave larger amplitudes than non-mother women. Basedon previous studies [2, 8], we expected that such characteristics of mothers would be more clearly observed in
the left hemisphere.
b) If the level of parental stress of mothers of infants
correlates with their behavioral inhibition-related brain
activity following recognition of emotions, there should
be a correlation between the total PSI score of mothers
and their Nogo-N2 and Nogo-P3 amplitudes.

Methods
Participants

Twenty-four healthy Japanese females participated in theexperiment. Of these, 13 females were engaged in raising
their biological child who was 3 years old or under (themother group) and 11 females had never experienced
pregnancy, child birth, or child rearing (the non-mothergroup). The ages of the mother group and non-mothergroup were 35.9 ± 2.29 (mean ± SD) years old and 27.2 ±2.89 years old, respectively. Responses to a questionnaire
indicated that the mother group had normal affection
for their biological child. The participants received anadequate verbal/written explanation of the experiment,
agreed to participate in the experiment, and signed aHayashi et al. Journal of Physiological Anthropology (2018) 37:8

written consent form before participating in the measurement. This experiment was carried out with approvalof the Ethics Committee of Kyushu University.
Stimuli and task

Pictures of facial expressions from 10 adults (five males
and five females) selected from the Karolinska Directed
Emotional Faces (KDEF) set [17] were used as the stimuli presented in the task. In consideration of a preceding
study [18], pictures of these 10 actors (angry/happy/neutral faces) were selected as stimuli. The pictures of thesefaces were cropped to an elliptical shape to eliminate theinfluence of hair and background cues (Fig. 1). Each facesubtended a visual angle of approximately 4° × 3°. The
task comprised of six blocks, with each block consistingof two categories of facial expression pictures: angryhappy/angry-neutral/happy-angry/happy-neutral/neutralangry/neutral-happy. In each stimulus pair, one was used
as a Go stimulus and the other was used as a Nogo stimulus. For example, in the pair of “angry-happy”, angry isused as a Go stimulus and happy as a Nogo stimulus in
one block. The participants were given instructions topress a button as soon as possible with the index finger of
their right hand which was their dominant hand when a
Go stimulus was presented and to withhold a responsewhen a Nogo stimulus was presented. Just before starting
each block, the participants were informed which emotional expression was a Go stimulus and which was aNogo stimulus. Each block contained 120 trials, of which
90 trials (75%) were Go and 30 trials (25%) were Nogo.
The order of the blocks and the order of the trials wererandomized between the subjects. Each stimulus was presented for 500 ms, with an inter-trial interval of 1750 ±250 ms. Presentation Ver. 18.1 (Neurobehavioral Systems,
Inc., USA) was used to present stimuli during the task.
Questionnaire

As a questionnaire form to measure parental stress, theJapanese version of the Parental Stress Index (PSI) form
[16] was used. The PSI is an academic tool developed by

Fig. 1 Example of the stimuli used in the emotional Go/Nogo task.
These pictures are the example of the facial stimuli used in this study.
The task included images of angry, happy, and neutral faces

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Abidin in 1980s to measure parental stress of mothers,
and the Japanese version of the PSI form was redeveloped to modify the original PSI suitable for Japaneseparents. It contains 78 items, consisting of 38 items and7 subscales to measure the stress related to characteristics of children (Child Domain) and 40 items and 8 subscales to measure the stress related to parents
themselves (Parent Domain). The total PSI score summing the scores from all the items was used as an index
of the overall parental stress of the mother group.
Procedure

The experiment was carried out in a sound attenuatingand electromagnetic wave shielded artificial climate
room. First, the participants were seated in a chair in theexperiment room and received an explanation of theexperiment. Next, they performed practice trials to become familiar with the task. Then, the task and concurrent electroencephalogram (EEG) measurement werecarried out. During the task, adequate breaks were taken
between trials if needed. After the task, the mothergroup participants answered the PSI questionnaire.
Recording and analysis of data

Task response times and answers were recorded using
Presentation Ver. 18.1 (Neurobehavioral Systems, Inc.).
Response times and percentage of correct responses
were computed from the recorded data. Response time
was defined as the time elapsed from Go stimulus presentation to pressing the button, and percentage of correct responses was defined as the number of successful
trials divided by the number of total trials under each facial expression (angry, happy, neutral). Trials wereregarded as successful if the button was pressed 100 to1000 ms after a Go stimulus presentation, and if the button was not pressed between 0 and 1000 ms after a
Nogo stimulus presentation. Other trials were regarded
as errors and excluded from the analysis.
EEG was recorded with a 64-channel EEG cap (64channel HydroCel GSN; Electrical Geodesics Inc., USA).
The EEG signals were amplified by a biological amplifier(Net Amps 200 64-channel EEG Amplifier; Electrical
Geodesics Inc.) and were recorded using specialized software (Net Station, ver. 4.1.2; Electrical Geodesics Inc.).
During the measurement, EEG was continuously recorded at a sampling frequency of 250 Hz with the impedance of electrodes kept at 100 kΩ or less. The lowcut and high-cut frequencies of the hardware filter were
set to 0.1 Hz to 100 Hz, respectively. Although a lower
cutoff frequency (e.g., 0.01 Hz) is usually recommended
for ERP experiments, the current setting was acceptableand often used with a high-impedance recording system
like the one we used. A reference electrode was locatedat Cz in the International 10-20 system.

Hayashi et al. Journal of Physiological Anthropology (2018) 37:8

EEG interpretation software (EMSE Data Editor 5.5.2;
Source Signal Imaging Inc., USA) was used for the analysis of the measured EEG data. In the preprocessing
stage, EEG signals from electrodes near the ears andcheeks containing artifacts were excluded from the analysis. The average potential of the remaining 58 electrodes was used as a reference for the analysis. In
addition, EEG was filtered again offline with an IIR filter(12 dB/octave), with low-cut frequency of 0.5 Hz and ahigh-cut frequency of 30 Hz.
For the computation of ERPs, the epoch between
200 ms before and 800 ms after stimulus presentation was
set apart as a single trial. All of the individual trials under
one condition were averaged to obtain an ERP waveform,
excluding the ones with incorrect responses or with noise
visually inspected in the period between − 500 ms and1000 ms after stimulus onset (such as an eye blink andmuscle artifacts, EEG amplitudes outside the range of ±60 μV). Before calculating the mean of all the trials, waveforms were aligned to the average potential over the 200ms pre-stimulus epoch of each trial as the baseline. The
arithmetic mean number of trials used under each condition per member of the mother group was Angry-Nogo,
39.9, Happy-Nogo, 43.1, and Neutral-Nogo, 42.7. Those of
the non-mother group were Angry-Nogo, 43.0, HappyNogo, 39.4, and Neutral-Nogo, 43.4.

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Global field power (GFP) [19] was derived from thecomputed ERPs. Based on GFP and preceding studies,N2 and P3 were defined as the peak potential between
200 and 300 ms after stimulus presentation and theaverage potential between 400 and 600 ms after stimulus
presentation, respectively. Furthermore, three areas located at the fronto-central region (FCz 3, 4, 6, 7, 9; 54,
FC3 11, 12, 13, 14, 15, 19; FC4 2, 53, 56, 57, 59, 60) wereset as areas of interest, and N2 and P3 amplitudes inthese three areas were computed (Figs. 2 and 3).
The PSI questionnaire was administered and scored inaccordance with the methods explained in the Manual
for the Japanese version of Parental Stress Index, andthen the total PSI score was calculated.
Statistical analysis

When computing ERPs, it was found that the total number of trials under certain condition was less than 20 forsome participants (four participants from the mothergroup and two participants from the non-mother group).
The data of these participants was excluded from thestatistical analysis, leaving the data of nine participantsfrom the mother group (36.0 years old ±1.93) and thedata of nine participants from the non-mother group(26.6 years old ±2.82) for the subsequent statistical analysis. There was a statistical difference in the age of theFig. 2 Electrode positions and three areas of interest. The blue, red, and orange solid-line circles indicate three areas of interest at the fronto-central
region (FCz, FC3, and FC4, respectively). FCz, FC3, and FC4 mean the areas of interest around FCz, FC3, and FC4 according to the 10-20 system

Hayashi et al. Journal of Physiological Anthropology (2018) 37:8

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Fig. 3 Average ERP waveforms and N2 and P3 components in each area of interest. The black line and the blue line indicate waveforms of themother group and non-mother group respectively. The solid line, dashed line, and a dashed-dotted line indicate waveforms elicited by angry,
happy, and neutral faces respectively. The peak amplitude between 200 and 300 ms and the average amplitude in the epoch between 400 and
600 ms were defined as N2 component and P3 component respectively

two groups (p < 0.001). All of them were right-handed
and had normal or corrected to normal vison. The ageof the children of the mothers was 25.5 ± 13.9 months(mean ± SD). All of the mother group were married andlived with their husbands and children. There was no
participant who was feeding her child only throughbreast-feeding.
A three-way analysis of variance (ANOVA) was
performed with group (mothers/non-mothers), emotion(angry/happy/neutral), and brain area (FC3/FCz/FC4) asfactors influencing Nogo-N2 and Nogo-P3 amplitudes.
A two-way ANOVA also was performed with group andemotion as factors influencing response time. Degrees of
freedom were corrected with the Greenhouse-Geisser
method. The Bonferroni-Holm method was used toadjust the P value during post hoc tests. In addition,
Pearson’s correlation coefficients were calculated for the
PSI and ERP components under each condition. Noncorrelation tests were performed upon the calculated
correlation coefficients to confirm the significance of thecorrelation. All of the significance levels for these tests
were set to 5%.

Results
Behavioral data
Percentage of correct responses

The mean percentages of correct responses of the mothergroup and of the non-mother group were 0.95 ± 0.07
(mean value±SD) and 0.94 ± 0.11, respectively (Table 1). A
three-way ANOVA was performed on group, trial, andemotion as factors affecting the percentages of correct
responses, which revealed a main effect of trial (F(1,16) =34.9, p < 0.001). Emotion had a main effect (F(2,32) = 10.5,
p = 0.001), and the percentages of correct responses toangry faces were lower than those to other faces (angry vsneutral: t(16) = 3.80, adj.p = 0.001, angry vs happy: t(16) =3.40, adj.p = 0.007). There were no significant main orinteraction effects of the group.
Response time

With respect to the response time to correct Go trials, a
two-way ANOVA was performed on group and emotion
as factors, which revealed a significant main effect ofemotion (F(2,32) = 3.87, p = 0.041) (Table 2). The multiple comparison test was performed for the further analysis of the main effect of emotion, but this revealed nosignificant result. There were no significant main orinteraction effects of the group.
ERP data
Nogo-N2

A three-way ANOVA was performed with group(mothers/non-mothers), emotion (angry/happy/neutral),and area (FC3/FCz/FC4) as factors affecting the NogoN2 amplitudes (Fig. 4). Area was revealed to have a main
effect (F(2,32) = 6.73, p = 0.005). A post hoc test revealed
that the Nogo-N2 amplitudes in FCz were larger thanthe other two areas (FCz vs FC3: t(16) = 2.48, adj.p = 0.
049, FCz vs FC4: t(16) = 3.25, adj.p = 0.015). There wasno significant difference between FC3 and FC4 (t(16) =1.54, adj.p = 0.143). Emotion had a main effect (F(2,32)= 4.84, p = 0.020), and the Nogo-N2 amplitudes evokedby happy faces were smaller than the Nogo-N2 amplitudes by neutral faces (t(16) = 3.90, adj.p = 0.004). ThereHayashi et al. Journal of Physiological Anthropology (2018) 37:8

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Table 1 The means and SDs of percentage of correct responses
Percentage of correct
responses (%)

Nogo trials
Angry

Happy

Neutral

Angry

Go trials
Happy

NeutralThe mother group87.0 (8.7)

88.9 (6.0)

91.2 (7.5)

93.5 (3.5)

99.5 (0.6)

98.1 (2.4)

The non-mother group79.1 (12.1)

82.3 (8.3)

82.5 (9.4)

96.5 (5.0)

98.8 (1.7)

97.8 (3.3)

Notes: Data are mean (SD)were no significant main or interaction effects of thegroup.
Nogo-P3

A three-way ANOVA was performed with group (mothers/
non-mothers), emotion (angry/happy/neutral) and area
(FC3/FCz/FC4) as factors affecting the Nogo-P3 amplitudes(Fig. 5). Group was observed to have a main effect (F(1,16)= 8.45, p = 0.010), with the Nogo-P3 amplitudes of themother group being larger than those of the non-mothergroup. Area also had a main effect (F(2,32) = 17.32, p < 0.
001). A post hoc test was performed, which revealed theNogo-P3 amplitudes in FCz and FC3 were larger than FC4(FCz vs FC4: t(16) = 6.06, adj.p < 0.001, FC3 vs FC4: t(16) =3.60, adj.p = 0.005). There was no significant difference
between FCz and FC3 (t(16) = 1.32, adj.p = 0.205). A marginally significant interaction effect between emotion andgroup was observed (F(2.32) = 2.51, p = 0.074). Post hoc
tests showed that the Nogo-P3 amplitudes evoked by angry
faces were larger than the Nogo-P3 amplitudes evoked by
the other two emotions only in FC3 (Angry vs Neutral:t(16) = 2.68, adj.p = 0.049, Angry vs Happy: t(16) = 2.63, adj.
p = 0.049). There was no significant difference between the
Nogo-P3 amplitudes elicited by happy and neutral faces(t(16) = 0.30, adj.p = 0.769). Other interaction effects were
not significant.
We additionally performed a three-way ANOVA withgroup, trial, and emotion as factors affecting the Go-P3
amplitudes. Area was observed to have a main effect(F(2.32) = 5.45, p = 0.014), with the Go-P3 amplitudes in
FCz which were larger than FC4 (t(16) = 3.16, adj.p < 0.
018). Group had a marginally significant main effect;
however, it was not significant (F(1.16) = 4.00, p = 0.063).
Other main or interaction effects were not significant.

regarding the total PSI score and ERP components ineach area under each condition. The results revealed asignificant negative correlation between the total PSI
score and the Nogo-P3 amplitude in FC3 evoked byangry faces (r2 = 0.47, p = 0.042) (Fig. 6). There was no
significant correlation between the total PSI score andother ERP components.

Discussion
With regard to the first hypothesis, a difference between
mothers and non-mothers was clearly shown in thelarger Nogo-P3 amplitude of the mother group (Fig. 5).
This result suggests that there is a difference between
the processing of mothers and non-mother women thatis reflected in the Nogo-P3 amplitude. Considering theresult that the Nogo-P3 amplitudes elicited by angry
faces were larger than the other faces only in FC3, theNogo-P3 amplitude would seem to reflect not only brain
activities inhibiting recognition and behavior following
presentation of emotional stimuli [13], but also processes related to emotion. This idea is in line with a previous study which suggests that Nogo-P3 amplitudes
overlap with the automatic response inhibition of emotions during implicit emotional tasks [20]. This interpretation does not contradict previous neuroimaging studiesof emotion regulation and maternal brain activity [2, 8].
However, we should be careful because the present study
did not perform source analysis and because there are few

Correlation between parental stress and ERP components

The average total PSI score of the mother group was
167.7 ± 30.6, and all participants reported a score within
the normal range. Pearson’s correlation coefficients werecomputed and non-correlation tests were performed
Table 2 The means and SDs of response times in correct Go trials
Response times (ms)

Angry

Happy

NeutralThe mother group418.6 (53.1)

398.3 (23.7)

414.9 (31.8)

The non-mother group442.5 (52.6)

421.1 (57.1)

428.6 (57.9)

Notes: Data are mean (SD)Fig. 4 Nogo-N2 amplitudes in FC3. The gray column and the blue
column indicate data of the mother group and the non-mother grouprespectively. The Nogo-N2 amplitudes evoked by happy faces were
smaller than the Nogo-N2 amplitudes by neutral faces. *p < 0.05

Hayashi et al. Journal of Physiological Anthropology (2018) 37:8

Fig. 5 Nogo-P3 amplitudes in FCz. The gray column and the blue
column indicate data of the mother group and the non-mother grouprespectively. The Nogo-P3 of the mother group were larger than thoseof the non-mother group. Only in the FC3, the Nogo-P3 evoked byangry faces were larger than those by other two emotions. *p < 0.05,**p < 0.01, ***p < 0.001

previous studies about left-right differences in ERP during
emotional Go/Nogo tasks.
Based on previous studies focused on maternal brain
activities, especially emotion regulation of mothers [1,2], we expected that the differences between mothers
and non-mothers would be enhanced in negative
emotional conditions. However, the results of this study
indicate that the Nogo-P3 amplitudes of mothers werelarger than those of non-mothers, regardless of theemotion of the facial stimuli. Thus, when inhibiting impulsive behavior, mothers may tend to exhibit greater
brain activity related to inhibition. It is reported that impulse control disability in mothers is related to childFig. 6 Correlation between PSI and Nogo-P3 amplitude in FC3
evoked by angry faces. □ indicates the data of each participant in
the mother group. The vertical axis and the horizontal axis represent
the Nogo-P3 amplitude evoked by angry faces in FC3 and the total
PSI score respectively. There was a negative correlation between themother group’s total PSI score and the Nogo-P3 amplitude in FC3
evoked by angry faces

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maltreatment [21], and it has been suggested that stressduring childhood including child maltreatment potentially leads to long-term changes in learning, behavior,and physiology that result in higher levels of stressrelated chronic diseases or the prevalence of unhealthy
lifestyles [22]. The importance of impulse control ability
in mothers may have a connection with the enhanced
Nogo-P3 amplitudes in mothers observed here.
With regard to the second hypothesis, association between the mother group’s parental stress and inhibitory
brain activity when emotions of others are recognized
was supported by the negative correlation between the
total PSI score and the Nogo-P3 amplitude when angry
faces were presented as the Nogo stimulus (Fig. 6). This
indicates that there may be an association between ahigh level of overall parental stress and a low level ofbrain activity inhibiting recognition and behavior in
response to angry faces. These inhibitory brain activities
may be associated with inhibitory control and emotional
intelligence, which are important for human social behavior [23]. Considering these, parental stress in mothersof infants may be associated also with social behavior of
mothers. This point would be possible to extend tomothers displaying an abnormal parental stress score as
well, and need further investigation in the future.
There are some limitations to the reliability of thisstudy. First, the lifestyle (for example, living together oralone and sleeping habits), age, and menstrual cycle in
the two groups were not controlled. It was too difficult
to control these because these are related to characteristics of mothers, who for example take care of their children day and night. However, these factors should becontrolled in subsequent studies if possible. Second, thenumber of participants may not have been sufficient. It
is almost the same as some previous studies whichinvestigated the differences between mothers and nonmother women, for example, Proverbio et al. [24], but it
is advisable to use more participants [25]. This study has
weaknesses regarding group selection and sample size,
but it may be the first study indicating that mothers
exhibit greater brain activity related to inhibition when
inhibiting impulsive behavior in response to emotionaland non-emotional stimuli than non-mother women.
This study should be useful as a preliminary study in thearea of emotion regulation by mothers.

Conclusions
The results of this study revealed that mothers and nonmother women have differences in their emotion regulation, especially in brain activity associated with behavioral
inhibition. The difference was clearly observed in Nogo-P3
amplitudes during the Go/Nogo task with emotional stimuli. This indicates that compared to non-mother women,mothers have greater brain activity inhibiting recognition

Hayashi et al. Journal of Physiological Anthropology (2018) 37:8

and behavior while performing appropriate behavior (inhibiting inappropriate behavior) in response to facial expressions of others. In addition, there was an association
between a high level of parental stress and a low level of behavior inhibition-related brain activity in response to angry
faces, suggesting that parental stress of mothers of infants
may be associated with social behavior of mothers.
Abbreviations
ANOVA: Analysis of variance; EEG: Electroencephalogram; ERPs: Event-related
potentials; GFP: Global field power; KDEF: The Karolinska Directed Emotional
Faces; PSI: The Parental Stress Index

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6.
7.
8.
9.
10.

11.
12.

Funding
This research did not receive any specific grant from funding agencies in the
public, commercial, or not-for-profit sectors.

13.

Availability of data and materials
The datasets during and/or analyzed during the current study are available
from the corresponding author on reasonable request.

14.

Authors’ contributions
SHa, HW, and YK contributed to the design of the experiment. SHa and HW
performed the experiments.SHa analyzed the data and wrote the manuscriptwith advice from YK and SHi. YM and SK participated in the discussion andpreparation of the manuscript. All authors read and approved the final
manuscript.
Ethics approval and consent to participate
The present study was performed according to the protocol that wasapproved by the Ethics Committee of Kyushu University (Approval No. 260).
All the subjects of this study gave their written informed consent toparticipate in this study.

15.

16.
17.
18.

19.

20.

Consent for publication
Not applicable.

21.

Competing interests
The authors declare that they have no competing interests.

22.
23.

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims in publishedmaps and institutional affiliations.
Author details
1
Department of Kansei Science, Graduate School of Integrated Frontier
Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581,
Japan. 2Department of Human Factors Engineering, Ulsan National Instituteof Science and Technology, 50 UNIST-gil, Eonyang-eup, Ulju-gun, Ulsan,
Republic of Korea. 3Department of Human Science, Faculty of Design,
Kyushu University, 4-9-1 Shiobaru, Minamiku, Fukuoka 815-8540, Japan.

24.

25.

Kikuchi Y, Noriuchi M. The neuroscience of maternal love. Neurosci
Commun. 2016;1:e991.
Musser ED, Kaiser-Laurent H, Ablow JC. The neural correlates of maternalsensitivity: an fMRI study. Dev Cogn Neurosci. 2012;2:428–36.
Laurent HK, Ablow JC. The missing link: mothers’ neural response to infant cry
related to infant attachment behaviors. Infant Behav Dev JAI. 2012;35:761–72.
Roelofs K, Minelli A, Mars RB, van Peer J, Toni I. On the neural control ofsocial emotional behavior. Soc Cogn Affect Neurosci. 2009;4:50–8.
Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontalsubcortical pathways mediating successful emotion regulation. Neuron.
2008;59:1037–50.
Ramnani N, Owen AM. Anterior prefrontal cortex: insights into function
from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5:184–94.
Donkers FCL, van Boxtel GJM. The N2 in go/no-go tasks reflects conflictmonitoring not response inhibition. Brain Cogn. 2004;56:165–76.
Nieuwenhuis S, Yeung N, van den Wildenberg W, Ridderinkhof KR.
Electrophysiological correlates of anterior cingulate function in a go/no-go
task: effects of response conflict and trial type frequency. Cogn Affect Behav
Neurosci. 2003;3:17–26.
Smith JL, Johnstone SJ, Barry RJ. Movement-related potentials in the go/
NoGo task: the P3 reflects both cognitive and motor inhibition. Clin
Neurophysiol. 2008;119:704–14.
Messerotti Benvenuti S, Sarlo M, Buodo G, Mento G, Palomba D. Influenceof impulsiveness on emotional modulation of response inhibition: an ERP
study. Clin Neurophysiol. 2015;126:1915–25.
Miho N, Yuriko K, Akiko A, MItsue M, Nobue N, Junko T, et al. Validity and reliabilityof the Japanese version of the parenting stress index. J Child Heal. 1999;58:610–6.
Lundqvist D, Flykt A, Öhman A. The Karolinska Directed Emotional Faces
set—KDEF; 1998. p. 3–5.
Euser AS, Franken IHA. Alcohol affects the emotional modulation of
cognitive control: an event-related brain potential study.
Psychopharmacology. 2012;222:459–76.
Hamburger HL, vd Burgt MAG. Global field power measurement versus
classical method in the determination of the latency of evoked potential
components. Brain Topogr. 1991;3:391–6.
Zhang W, Lu J. Time course of automatic emotion regulation during a facial
Go/Nogo task. Biol Psychol. 2012;89:444–9.
Tachibana Y, Takehara K, Kakee N, Mikami M, Inoue E, Mori R, et al. Maternal
impulse control disability and developmental disorder traits are risk factors
for child maltreatment. Sci Rep Nature Publishing Group. 2017;7:15565.
Shonkoff JP, Garner AS. The lifelong effects of early childhood adversity and591 toxic stress. Pediatrics. Am Acad Pediatr. 2012;129:e232-e246.
Köchel A, Leutgeb V, Schienle A. Affective inhibitory control in adults withattention deficit hyperactivity disorder: abnormalities in electrocortical latepositivity. Neurosci Lett. 2012;530:47–52.
Proverbio AM, Brignone V, Matarazzo S, Del Zotto M, Zani A. Gender andparental status affect the visual cortical response to infant facial expression.
Neuropsychologia. 2006;44:2987–99.
Simmons JP, Nelson LD, Simonsohn U. False-positive psychology:
undisclosed flexibility in data collection and analysis allows presenting
anything as significant. Psychol Sci. 2011;22:1359–66.

Received: 30 August 2017 Accepted: 13 March 2018

References
1. Kim P, Strathearn L, Swain JE. The maternal brain and its plasticity inhumans. Horm Behav. 2016;77:113–23.
2. Rilling JK. The neural and hormonal bases of human parental care.
Neuropsychologia. 2013;51:731–47.
3. Crandall A, Deater-Deckard K, Riley AW. Maternal emotion and cognitive
control capacities and parenting: a conceptual framework. Dev Rev.
2015;36:105–26.
4. Seifritz E, Esposito F, Neuhoff JG, Lüthi A, Mustovic H, Dammann G, et al.
Differential sex-independent amygdala response to infant crying andlaughing in parents versus nonparents. Biol Psychiatry. 2003;54:1367–75.
5. Kikuchi Y, Noriuchi M. Emotional engineering volume 4. In: Fukuda S, editor.
Emot. Eng. Vol. 4. Springer International Publishing; 2016. p. 189–198.

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