Reviewer #1:
Review title: The neural influence of autobiographical memory related to the parent-child
relationship on psychological health in adulthood
The current paper investigates the brain regions associated with the recall of autobiographical
memories of peoples’ childhood memories of parental facial expressions in certain
childhood situations. Specifically, looking into the association between current psychological
health (self-esteem, anxiety, and depression), quality of parent-child-relationship,
and specific brain regions activities.
Overall: The paper is a very interesting study and there is potential for novel information.
The biggest criticisms are the characterization of the task as an autobiographical
memory retrieval task, the lack of clear theory, and the major reverse inferencing
due to a lack of supporting measures. Additional data is needed to support any of
the claims the authors make.
Reply:
We greatly appreciate the positive evaluation and valuable comments on the manuscript
revision. Problems pointed out were all reflected in the revision of the manuscript.
Introduction: The introduction needs a rewrite. The paper is bit hard to follow. The
authors in a single paragraph talk about several topics, e.g., emotion regulation,
global-self-esteem, anxiety, depression, memory biases, etc. Each topic should be
within its own paragraph/section. One section can be on self-esteem and memory, anxiety
and memory, etc.
Reply:
As suggested, the introduction was totally rewritten. Autobiographical memory, memory
biases, self-esteem, depression, and anxiety were described as separate paragraphs
and contents were supplemented. The emotion regulation-related content was deleted
because it did not fit the subject of this paper. In addition, we added some additional
background on the nature of parental roles and how processing fathers and mothers
engage the brain differently.
Revision:
In ‘the first to 7th paragraphs’ of the Introduction section
Like the saying, “no health without mental health,” promoted by the WHO, psychological
health or psychological well-being is a fundamental factor contributing to quality
of life [1]. There are many factors that influence psychological health in adulthood,
and one of the most central determinants is the parent-child relationship [2]. The
relationship between a parent and child becomes the template for other interpersonal
relationships because attachment bonding allows a person to understand their environment
and establish a sense of security [3,4]. An examination of the association between
the retrospective perceptions of the parent-child relationship and emotional health
in adulthood showed that daily emotional and psychological distress are closely related
to how one perceives the quality of the parent-child relationship, and the retrospective
perceptions of father-child and mother-child relationships contribute to different
dimensions of emotional health [5]. Therefore, the perceptions of the childhood relationship
with parents are important in the overall well-being, even as adults.
The retrospective perceptions of the parent-child relationship are based on an individual’s
autobiographical memory. The development of autobiographical memory is a social process
that is influenced by the reminiscing style of parents, and thus an integral part
of the developing sense of self and interpersonal relatedness [6,7]. Autobiographical
memory represents the self and shapes emotional states of our everyday lives [8,9].
In general, memories are highly intertwined with features like self-referential processing
and emotion [9]. Functional neuroimaging studies have examined autobiographical memories
in reference to other types of memories. For instance, a recent study that compared
the difference between autobiographical memory and simple recognition memory found
that when a task required retrieval of life memories, default-mode areas were engaged
more, whereas a simple recollection of memories engaged the parietal memory network
[10]. Since autobiographical memory retrieval relies heavily on self-reference and
emotion, retrieval of autobiographical memories has been shown to employ various cortical
and subcortical regions, including the prefrontal and parietal cortices, anterior
cingulate cortex (ACC), precuneus, medial temporal cortex, hippocampus, and amygdala
[11-14]. In particular, the amygdala has been implicated in the encoding of emotional
memories [15] as well as retrieval of autobiographical memories [16]. Previous studies
also found coactivation of the amygdala, hippocampus, and inferior frontal gyrus (IFG)
during the retrieval of autobiographical memories [17] and neural responses in the
dorsal to caudal ACC and IFG elicited by the retrieval of painful autobiographical
memories [18]. These reports consistently show a close relationship between autobiographical
memory and emotional memory.
Psychological health is very closely related to memory encoding and retrieval, and
there is evidence supporting its influence on neural activities related to autobiographical
memory. Numerous studies have also shown the connection between psychological health
and selective memory bias. The representation, recall, and maintenance of autobiographical
memories have shown to be disturbed by individuals with poor psychological well-being,
where they are systematically biased for negative information [11]. Memory bias and
negative interpretations of events contribute to a vicious cycle, where one’s psychological
health contributes to the tendency toward negative interpretation of memories, and
this bias also maintains low self-esteem, depression, or anxiety [19-21]. In fact,
there is a consensus that self-esteem, anxiety, and depression are core elements of
psychological health [22-24]. The importance of these elements has spurred researchers
to study the close associations between self-esteem, anxiety and depression, and quality
of life in numerous fields [25-28].
Self-esteem is a facet of personality that affects perception of social standing and
modulates the salience of social interaction. Previous studies have shown that the
midline cortical structures, such as the medial prefrontal cortex (PFC), ACC, posterior
cingulate cortex (PCC), and precuneus that mediate self-referential processing are
also closely involved in the expression of self-esteem [29]. Global self-esteem, which
includes self-competence and self-liking, is related to selective memory, especially
toward a negatively salient stimulus [19]. Individuals with lower self-esteem tend
to be more concerned with how others perceive them, and this makes heightened negative
events more memorable. Lower self-esteem predicts an increase in ventral ACC and medial
PFC activity in response to positive versus negative social feedback, indicating the
relationship between self-esteem and the salience processing [30]. On the other hand,
a positivity bias for events that involve self-evaluations is stronger for individuals
with higher self-esteem, suggesting that this bias affecting autobiographical memory
is part of psychological mechanisms for maintaining a positive self-image [31]. The
underlying neural substrates of a positive self-evaluation include the medial ventral
and dorsolateral PFC and hippocampus, reflecting cognitive effort and emotional involvement
for the positivity bias [32]. In addition, it has been reported that the lateral PFC,
dorsal ACC, posterior cingulate cortex (PCC), precuneus, and caudate are involved
in negative or positive character feedback associated with self-esteem [33].
The level of self-esteem may be related to the manifestation of depression through
memory biases [34]. Many studies have reported that overall autobiographical memory
predicts the onset or course of depression and thus is considered to be a risk factor
for depression [35,36]. Depression contributes to the deviant reactivation of neural
areas associated with autobiographical memory retrieval [37]. Neural correlates of
autobiographical memory deficits in depressed patients have been known to involve
a wide range of brain regions, such as the IFG, lateral orbitofrontal cortex (OFC),
dorsomedial and ventrolateral PFC, ACC, precuneus, temporoparietal cortex, insula,
hippocampus, and amygdala [38-40].
Pathological anxiety has also been associated with negative memory bias [41]. Like
depression, anxiety disorders are also characterized by maladaptive emotional responses
and retrieval of memories [42]. In particular, negative autobiographical memory bias
is prominent in individuals high in social anxiety [43]. Increased state anxiety decreases
the ability to retrieve specific autobiographical memory [44]. Previous studies of
patients with anxiety disorders have reported functional impairments of structures
linked to the experience and regulation of emotion, such as the PFC, ACC, insula,
and amygdala [45-47].
Although behavioral and neurobiological studies indicate the impact of the psychological
dimensions on the encoding and retrieval of autobiographical memories, the way in
which psychological health affects memory processes in the general population is still
unknown. The importance of the parent-child relationship in child development has
been well documented. When looking at the way parents interact with a child, mothers
are often more caring and nurturing, whereas fathers engage in more playful interactions
[48]. Naturally, since the relationship between a father and child is different from
the relationship between a mother and child, the autobiographical memories of parents
in adulthood must be different. This difference is also observed in the brain response.
For example, faces of mothers elicited more activity in the face processing network
including the fusiform gyrus, whereas faces of fathers elicited more activity in the
striatal region [49]. Despite the importance of the parent-child relationship and
its difference between parents, no study has provided neurobiological evidence for
how perceptions change depending on the parent and the valence of memories.
Also, explaining more in-depth of the specific brain regions associated with the recall
of autobiographical memories, emotional memories, since this is the specific task
participants will be engaging in.
Reply:
As suggested, additional explanations regarding autobiographical memory and emotional
memory were added to a separate paragraph.
Revision:
In ‘the second paragraph’ of the Introduction section
The retrospective perceptions of the parent-child relationship are based on an individual’s
autobiographical memory. The development of autobiographical memory is a social process
that is influenced by the reminiscing style of parents, and thus an integral part
of the developing sense of self and interpersonal relatedness [6,7]. Autobiographical
memory represents the self and shapes emotional states of our everyday lives [8,9].
In general, memories are highly intertwined with features like self-referential processing
and emotion [9]. Functional neuroimaging studies have examined autobiographical memories
in reference to other types of memories. For instance, a recent study that compared
the difference between autobiographical memory and simple recognition memory found
that when a task required retrieval of life memories, default-mode areas were engaged
more, whereas a simple recollection of memories engaged the parietal memory network
[10]. Since autobiographical memory retrieval relies heavily on self-reference and
emotion, retrieval of autobiographical memories has been shown to employ various cortical
and subcortical regions, including the prefrontal and parietal cortices, anterior
cingulate cortex (ACC), precuneus, medial temporal cortex, hippocampus, and amygdala
[11-14]. In particular, the amygdala has been implicated in the encoding of emotional
memories [15] as well as retrieval of autobiographical memories [16]. Previous studies
also found coactivation of the amygdala, hippocampus, and inferior frontal gyrus (IFG)
during the retrieval of autobiographical memories [17] and neural responses in the
dorsal to caudal ACC and IFG elicited by the retrieval of painful autobiographical
memories [18]. These reports consistently show a close relationship between autobiographical
memory and emotional memory.
Also, the hypothesis of this paper are also not clear. For example, “We predicted
that emotional ratings would be correlated with psychological health facets.” What
emotional ratings are being referenced? Rating of the specific parental facial expressions
expressed by a parent during a given encounter or the valence of the memory in general.
Furthermore, there was no justification for why they hypothesized different activity
in memory regions based on parent or emotion.
Reply:
We sincerely apologize for the confusion. To answer the first part, the “emotional
ratings” we mentioned in the hypothesis was the in-scan behavior data. In the revised
manuscript, the hypothesis was updated to avoid the confusion.
Revision:
In ‘the last paragraph’ of the Introduction section
In this study of the general population, we sought to identify the neural substrates
of the impression of parents while participants recalled childhood memories. For this
purpose, we examined how fathers and mothers are perceived differently and whether
the valence of memory influences this perception, and surveyed the effects of psychological
health (self-esteem, depression, and anxiety) on the memory process. As childhood
memories of parents triggered by various situations are inherently charged with emotions,
we hypothesized that regions often involved in an autobiographical memory, such as
the ACC, IFG, amygdala, and hippocampus, would be engaged differently depending on
the parent and the valence of situation, and would be modulated by a person’s psychological
health.
Methods: A concern of the study is whether participants actually engaged in autobiographical
memory recall rather than imagination or simply an impression. First, there is substantial
research showing that retrieving specific autobiographical memories takes more time
than 3 seconds in response to a cue word (see Conway, 2005)! In addition, participants
were not actually instructed to retrieve a memory, but rather to imagine their parents’
facial expression. This type of task will be heavily influenced by current/recent
experiences with their parents’ facial expression. Lastly, I’m not sure it is possible
to both retrieve a memory and make the facial judgment within 3 seconds. Because participants
were forced to respond so quickly (and did so looking at the RT’s), this task is best
interpreted as an impression task. Do the authors have any evidence to support their
interpretation of the task?
Reply:
We are sincerely grateful for this particular point. As indicated, 3 seconds can actually
be a very short time to remember an autobiographical memory. Our manuscript had no
basis to properly answer this pointed problem. Now, following your recommendations
at the end, we provided clarity data for task stimuli after the additional experiment.
As shown in the newly added Table 1, the vividness of memory associated with the situation
and the intensity of reaction received from a parent in all situations indicated 4
or greater, which means ‘above moderately.’ We think these results may explain to
an extent to what you have expressed concerns. In the revised manuscript, we added
this comment in the discussion.
Revision:
In ‘the first paragraph’ of the Discussion section
The three seconds given for the task may have been too short to remember an autobiographical
memory. However, since the vividness and reaction intensity in the stimulus assessments
were rated as moderately or higher, we can say that the task was to evoke an autobiographical
memory rather than an imagination or a simple impression.
The authors also report using a linear mixed model to analyze the behavior. First,
this model is quite complex and much more information is needed regarding how the
model was set up (first level, second level factors, etc) and why this model was chosen
over an ANOVA.
Reply:
As pointed out, it seems that LMM was not necessary, and thus ANOVA was applied to
the revised manuscript. As the analysis method changed, it was adjusted accordingly
to the statistical values of the results.
Revision:
In ‘Behavioral task and analysis’ of the Methods section
The ANOVA was used to identify the main effect of parents (father and mother) and
situation (positive, negative, and neutral) and the interaction effect between them.
In ‘Behavioral results’ of the RESULTS section
Figure 2 illustrates the mean imagined emotion score and mean RT in each condition
during the task. The imagined emotion scores showed a main effect of situation [F2,47
= 408.28, p < 0.001], but not a main effect of parents [F1,71 = 0.45, p = 0.504] and
a significant parents × situation interaction [F2,23 = 0.80, p = 0.460]. Post-hoc
analyses showed that the scores for the positive situations were significantly higher
than those for the negative (t = 20.49, p < 0.01) and neutral situations (t = 14.53,
p < 0.01), and the scores for the negative situations were significantly lower than
those for the neutral situations (t = -15.86, p < 0.01).
The RTs also showed a main effect of situation [F2,47 = 45.42, p < 0.001] and a significant
parents × situation interaction [F2,23 = 4.42, p = 0.024], but not a main effect of
parents [F1,71 = 0.06, p = 0.813]. Post-hoc analyses showed that the RTs for the positive
situations were significantly shorter than those for the negative situations (t =
-6.82, p < 0.01) and the neutral situations (t = -6.77, p < 0.01), and there was no
significant difference between the negative and neutral situations (t = 1.49, p =
0.151). The RTs in the father-negative condition were significantly longer than those
in the father-neutral condition (t = 3.90, p < 0.01), whereas there was no significant
difference between the mother-negative and mother-neutral conditions (t = 1.49, p
= 0.453).
Results: The authors should report all results and all p-values e.g. …”(t = 2.77,
p < 0.05)” (p. 9); “but showed no parent effect and a significant parents × situation
interaction.” (p. 8) Can the authors also show figures of the main effects? The authors
also do not appropriately describe the interactions (which are based on differences
between conditions). The authors’ worded the interaction as main effects (“ACC activity
was significantly greater in the father condition than in the mother condition”),
which were inaccurate.
Reply:
As suggested, we added statistics for the results without significance. Since the
differences among the positive, negative, and neutral conditions were so similar between
the father and mother conditions, we did not add a graph of the main effect to avoid
the duplication. In terms of the interaction effect, we agree with the comment that
our reports were inaccurate. In the revised results, we changed them into an appropriate
form.
Revision:
In ‘Behavioral results’ of the RESULTS section
Figure 2 illustrates the mean imagined emotion score and mean RT in each condition
during the task. The imagined emotion scores showed a main effect of situation [F2,47
= 408.28, p < 0.001], but not a main effect of parents [F1,71 = 0.45, p = 0.504] and
a significant parents × situation interaction [F2,23 = 0.80, p = 0.460]. Post-hoc
analyses showed that the scores for the positive situations were significantly higher
than those for the negative (t = 20.49, p < 0.01) and neutral situations (t = 14.53,
p < 0.01), and the scores for the negative situations were significantly lower than
those for the neutral situations (t = -15.86, p < 0.01).
The RTs also showed a main effect of situation [F2,47 = 45.42, p < 0.001] and a significant
parents × situation interaction [F2,23 = 4.42, p = 0.024], but not a main effect of
parents [F1,71 = 0.06, p = 0.813]. Post-hoc analyses showed that the RTs for the positive
situations were significantly shorter than those for the negative situations (t =
-6.82, p < 0.01) and the neutral situations (t = -6.77, p < 0.01), and there was no
significant difference between the negative and neutral situations (t = 1.49, p =
0.151). The RTs in the father-negative condition were significantly longer than those
in the father-neutral condition (t = 3.90, p < 0.01), whereas there was no significant
difference between the mother-negative and mother-neutral conditions (t = 1.49, p
= 0.453).
In ‘Imaging results’ of the RESULTS section
There was an interaction effect in the right caudal ACC and right precuneus. As shown
in Figure 3A, right caudal ACC activity in the father condition was significantly
greater in the negative situation than in the positive situation (t = 5.09, p < 0.01),
whereas that in the mother condition was not significant but greater in the positive
condition than in the negative condition (t = 1.34, p = 0.193). Figure 3B also shows
that right precuneus activity in the father condition was significantly greater in
the negative situation than in the positive situation (t = 2.35, p < 0.05), whereas
that in the mother condition was not significant but greater in the positive condition
than in the negative condition (t = 1.94, p = 0.065).
The authors should reconsider the names of their regions and interpretation. The ACC
activity they found is better characterized as mid cingulate cortex. It is a bit too
posterior to be considered dACC activity.
Reply:
We agree with this comment. I have two significant results in the ACC. In the revised
manuscript, the first one in the main effect of situation was named the dorsal ACC,
and the second one in the interaction effect was regarded as the caudal ACC. As a
result of this separation, the interpretation in the discussion was changed accordingly.
Revision:
In ‘Imaging results’ of the Results section
There was an interaction effect in the right caudal ACC and right precuneus.
In ‘3rd and 4th paragraphs’ of the Discussion section
From the neuroimaging data, we saw intriguing neural responses to each condition from
the right caudal ACC and precuneus, in particular. In the result of the caudal ACC,
there was a particular bias toward father-negative and mother-positive, suggesting
that in the autobiographical memory of emotional events, different forms of brain
reactions occur depending on the parent's gender. Attention on the caudal ACC has
risen in recent years and studies have indicated that the region contributes significantly
to negative affect and pain processing [56-58]. This region receives an ample amount
of emotion-related and voluntary movement signals [59,60], and has been suggested
as a pivotal site for the emotional and voluntary interaction [58]. In a fascinating
investigation on pain processing in self and others, it was seen that the caudal ACC
was activated in response to self-experienced pain, but not when perceiving pain in
others [56]. Furthermore, this region was shown to increase in response to negatively
charged autobiographical memories [61]. On the other hand, its involvement in other-experienced
pain processing has also been reported. A meta-analysis on empathy-related regions
indicates that this region is part of the pain empathy network, and is engaged when
pain was anticipated [62]. Regardless, it is clear that the caudal ACC plays a role
in processing negative affect.
In light of these caudal ACC functions, our results may be linked to mothers taking
on the role of primary caretaker more so than the fathers. In many cultures, traditional
gender roles have determined the roles and expectations for parents, which usually
assumes fathers as breadwinners and mothers as the primary caretaker in child rearing
[63,64]. This point can be related to our results of the stimulus assessment. The
analysis of the stimulus assessments indicated that the responses that fathers gave
were less intense in all situations than those given by mothers; and the imagination
of fathers’ appearances were less vivid and evoked less arousal than that of the mothers.
In these respects, it is possible that caudal ACC activity may be a response to the
stoic and emotionally distant perception of fathers. Meanwhile, the importance of
memory to the mother can be seen in our result of negative correlation between caudal
ACC activity in the mother-positive condition and depression score. There was a report
that pathological changes in this region may be related to major depressive disorder
[65]. A study on the behavioral adaptation to unpleasant environment showed the involvement
of the caudal ACC to be critical in the ability to regulate the behavior [66]. It
has been suggested that the region might contribute to defending one from developing
depression [67]. Taken together, our result of the negative correlation in the mother-positive
condition may suggest that through the function of the caudal ACC, autobiographical
memories of positive events with the mother may act as a factor that prevents depression.
Motivation for the correlations do not make sense. For example, the authors found
activity in the “ACC” that was driven by valence differences in the father condition,
and yet found a correlation between depression and brain activity in this region in
the mother-positive condition! Same with the other correlation. This implies that
the authors assessed all possible correlations, regardless as to whether they made
sense which would be at least 24 tests (3 scales, 4 conditions, 2 regions), thus inflating
false positives. Not only should these correlations not be trusted (due to false positives),
but they also were not hypothesized.
Reply:
As defined in the introduction, we hypothesized that a person’s psychological health
(self-esteem, anxiety, and depression) would be modulated by neural regions including
the ACC, IFG, hippocampus, amygdala, and other areas associated with autobiographical
memory recall. Since the regions of interest (caudal ACC and precuneus) result from
the interaction effect, we considered their activity meaningful in every condition.
We saw that if there was a difference in the father condition, there was also a meaning
of no difference in the mother condition, and vice versa. Of course, as pointed out,
it is a problem that the likelihood of false positives increases. We added this problem
in the limitation of the study in the discussion.
Revision:
In the 9th paragraph of the DISCUSSION section
Second, since the correlation analysis was performed between three scale scores and
regional activity under each condition, the possibility of false positives should
be considered in interpreting the results.
Discussion: The major issue in the discussion is that the authors over-interpret their
findings and use a lot of reverse inferencing to do so. As one example, the authors
claim that the dACC activity represents conflict processing. First, I am not convinced
that the dACC was activated at all. However, even if this were to be the dACC, the
dACC is one of the most active areas and does not indicate that conflict processing
has occurred. The authors would benefit from reading Poldrack, R. A. (2011). Inferring
mental states from neuroimaging data: from reverse inference to large-scale decoding.
Neuron, 72(5), 692-697. Another example is that the authors claim that they can “therefore
infer that the perceptions of fathers were more personal and vivid than those of mothers,
especially during reminiscence of negative situations.” Again, none of this can actually
be inferred without actual ratings of vividness or “personalness”. Because the Discussion
is primarily comprised of entirely reverse inferencing and over-interpretation, it
would have to be rewritten and I am convinced that nothing can be firmly concluded
without additional data.
One source of evidence of over-interpretation is again the interpretation of conflict
monitoring. Decades of research has shown that conflict comes with a cost in response
times. And yet, this “conflict monitoring” that occurs only for fathers and not mothers
is not borne out in the RT ratings.
Reply:
We agree with the comments that our discussion contained too much of over-interpretation.
As suggested, we included additional behavioral data in order to clarify certain claims
that we made. We also edited our claims to eliminate reverse inferencing and over-interpretation
as much as possible. Additionally, we changed the dACC region significant from the
interaction effect to the caudal ACC. Accordingly, the discussion section of the revised
manuscript was rewritten entirely.
Revision:
In ‘the 3rd to 8th paragraphs’ of the Discussion section
From the neuroimaging data, we saw intriguing neural responses to each condition from
the right caudal ACC and precuneus, in particular. In the result of the caudal ACC,
there was a particular bias toward father-negative and mother-positive, suggesting
that in the autobiographical memory of emotional events, different forms of brain
reactions occur depending on the parent's gender. Attention on the caudal ACC has
risen in recent years and studies have indicated that the region contributes significantly
to negative affect and pain processing [56-58]. This region receives an ample amount
of emotion-related and voluntary movement signals [59,60], and has been suggested
as a pivotal site for the emotional and voluntary interaction [58]. In a fascinating
investigation on pain processing in self and others, it was seen that the caudal ACC
was activated in response to self-experienced pain, but not when perceiving pain in
others [56]. Furthermore, this region was shown to increase in response to negatively
charged autobiographical memories [61]. On the other hand, its involvement in other-experienced
pain processing has also been reported. A meta-analysis on empathy-related regions
indicates that this region is part of the pain empathy network, and is engaged when
pain was anticipated [62]. Regardless, it is clear that the caudal ACC plays a role
in processing negative affect.
In light of these caudal ACC functions, our results may be linked to mothers taking
on the role of primary caretaker more so than the fathers. In many cultures, traditional
gender roles have determined the roles and expectations for parents, which usually
assumes fathers as breadwinners and mothers as the primary caretaker in child rearing
[63,64]. This point can be related to our results of the stimulus assessment. The
analysis of the stimulus assessments indicated that the responses that fathers gave
were less intense in all situations than those given by mothers; and the imagination
of fathers’ appearances were less vivid and evoked less arousal than that of the mothers.
In these respects, it is possible that caudal ACC activity may be a response to the
stoic and emotionally distant perception of fathers. Meanwhile, the importance of
memory to the mother can be seen in our result of negative correlation between caudal
ACC activity in the mother-positive condition and depression score. There was a report
that pathological changes in this region may be related to major depressive disorder
[65]. A study on the behavioral adaptation to unpleasant environment showed the involvement
of the caudal ACC to be critical in the ability to regulate the behavior [66]. It
has been suggested that the region might contribute to defending one from developing
depression [67]. Taken together, our result of the negative correlation in the mother-positive
condition may suggest that through the function of the caudal ACC, autobiographical
memories of positive events with the mother may act as a factor that prevents depression.
The precuneus, a central hub of the default mode network, also exhibited a similar
interaction effect between the parent and situation during the childhood memory recollection
task. The precuneus has been thought to play a critical role in episodic memory [68,69],
source monitoring [70], and self-referential processing [71]. Recently, a multivariate
analysis method, representational similarity analysis, demonstrated that the precuneus
is a key region engaged during the subjective experience of vivid autobiographical
memory reminiscence [72]. Other experiments have confirmed its prominent involvement
in the vividness of self-related memories [73,74]. In addition, right lateralization
of the precuneus has been shown for highly personal and vivid reminiscence of autobiographical
events [72]. Right lateralization is corroborated by the present study, which required
participants not only to visualize a given circumstance, but also to delineate the
facial expression by either parent. Our results indicate overall greater activation
of the right precuneus during recollection of fathers than mothers, and more specifically,
its activity was higher when recollecting fathers in negative compared to positive
situations. It is interesting to note that despite lower vividness score in the stimulus
assessments for fathers than mothers, these findings were observed, suggesting that
the perceptions of fathers may be more personal than those of mothers, especially
during reminiscence of negative situations. These may indicate the saliency of childhood
memories of fathers and particularly how fathers responded during negative circumstances.
In conjunction with activity of the caudal ACC, we cautiously conclude that memories
of fathers in negative situations have a more adverse effect as the negative impression
of fathers is more permanently embedded. This interpretation can also be linked to
the results of correlation with self-esteem.
Studies report that the neural structure of personal semantic memories serves as
a neural correlate of self-esteem [75,76]. It is postulated that due to its role in
using autobiographical memories to choose the applicable self-relevant information,
activation of the precuneus is closely related to self-esteem and how one processes
given information [76,77]. The current study confirmed the established association
between self-esteem and precuneus activity, as we found a negative relationship between
one’s self-esteem and precuneus activity during autobiographical reminiscence of fathers
in negative events. Recently, the precuneus was identified to correlate positively
with evaluation sensitivity, measured by a change in state self-esteem [75]. Together
with the evidence supporting the precuneus’ affiliation with evaluation sensitivity,
as well as the tendency for individuals with lower self-esteem to be more affected
by negative information [76], our result seems to suggest that the heightened activation
observed in individuals with lower self-esteem may be due to the saliency of negative
memories during recollection and their tendency to be more influenced by negative
information.
Our PPI analysis revealed significant increases in functional connectivity of the
caudal ACC with the fusiform gyrus and postcentral gyrus for the father-positive condition
compared to the mother-positive condition. Given that the fusiform gyrus processes
facial identity [78] and emotion [79], our finding may indicate that a greater sense
of negative affect was involved while processing facial expressions of fathers than
mothers in positive childhood events. This raises the possibility that the negative
affect arisen from processing emotional face expressions may be particularly different
between the parent in a positive context. Going back to the stimulus assessments,
we saw lower vividness, response intensity, and arousal from fathers than mothers.
Again, this may be since, generally, mothers are primary caregivers who spend more
time with children; thus, one may have more readily available positive memories involving
mothers than fathers to access on demand.
Previously, individuals with high trait anxiety have shown to hyperactivate the fusiform
gyrus while processing uncertain cues and angry faces [80,81]. Consistent with the
activation study, our study revealed that the connectivity strengths between the cingulate
cortex and fusiform gyrus during the father-positive versus mother-positive condition
correlated positively with the severity of anxiety symptoms. These results may provide
the neurobiological influence of trait anxiety in the retrieval of memory and the
perception of fathers. In addition to emotional face processing, greater connectivity
between the cingulate area and postcentral gyrus was witnessed for the father-positive
than mother-positive condition. Functional connectivity between these two regions
has been implicated in posttraumatic stress disorder (PTSD), where patients with PTSD
showed stronger connectivity than the control group, and also was positively correlated
with the severity of symptoms [82]. As part of the sensorimotor network [83], the
coupling of the caudal ACC and postcentral or paracentral gyri has been shown to be
involved in shock processing [84] and other emotional memory tasks [85]. Based on
the evidence, we postulate that the caudal ACC may relay negatively valenced affective
information to the sensorimotor area more for fathers than mothers when processing
facial expressions.
Lastly, the authors do indicate one of the major limitations is not being able to
analyze sex differences due to the small sample size (which I agree with), but the
authors may not realize how much of a problem this actually is. Because the authors
have already chosen to differentially investigate effect mother vs. father effects,
the relationship and memory biases that one might have will surely depend on the sex
of the individual. The net result is an average set of brain activity that may not
represent either the men or women (e.g., the average of 0 and 10 is 5 and 5 is equally
as far from representing men and women, nor represent either).
Reply:
We whole-heartedly agree with this comment on the importance of exploring the sex
differences in this study. Because we couldn't do it because of the small number of
samples, we added the reviewer's point as an additional description to the limitation
of the study.
Revision:
In the 9th paragraph of the DISCUSSION section
First, in the relationship with parents, the degree of intimacy or memory biases can
vary between father and mother, depending on the individual's sex. Because of the
small sample size, however, the effect of sex variation was not analyzed.
Recommendations: In the end, I would highly recommend testing a new set of participants
behaviorally in the same task, but with additional probing to test whether they actually
retrieved a memory, to rate the vividness of that memory, assess the degree of conflict
they experienced, and any other rating to support the inferences the authors are making.
Making claims of cognitive processing based on the neuroimaging findings alone without
such support is a critical and known inferencing flaw in the neuroimaging community.
Reply:
We greatly appreciate this suggestion on conducting additional tests. In fact, before
the experiment, we had performed a preliminary test to survey the intensity of reaction
given by a parent, the vividness of each stimulus, and the level of arousal to ensure
the validity of the task. However, due to the small number of subjects, the results
were not included in the manuscript. In response to the reviewer’s recommendation,
we carried out additional experiment to increase the number of subjects, and the data
has been included in the method and results to the revised manuscript. We believe
the results helped to mitigate the over-interpretation and reverse-inference problem,
and we thank you again for the comment.
Revision:
In ‘Task stimuli’ of the Methods section
Participants performed a task where they were asked to imagine what their parents’
facial expression looked like in a given situation during their childhood. Visual
stimuli with a grey background included black words presenting a situation in the
upper part and four black and white faces of the same person expressing different
emotions (very happy, a little happy, very angry, and a little angry) in the lower
part (Figure 1). The number of situations used in the task was 30, including ten positive
(e.g., when I did errands), ten negative (e.g., when I did not do homework), and ten
neutral (e.g., when I was on the phone). All actual situations used are shown in Supplementary
Table S1.
In order to evaluate the validity of the presented words, the vividness of memory
associated with the situation, the intensity of reaction received from a parent in
the situation, and the current degree of arousal caused by the recollection of the
situation were assessed for each situation in 24 volunteers who did not participate
in the fMRI experiment (27.3 ± 1.7 years old; 11 females and 13 males). Similar to
the fMRI task, each situation was presented with either word “Mother” or “Father”
on top of a page, then the volunteers were instructed to visualize an image of a parent
during their childhood. All three items (vividness, response intensity, and arousal)
were measured on a 9-point scale (0: not at all, 4: moderately, and 8: extremely).
Analysis was conducted using repeated measures ANOVA for parent (Mother and Father)
and valence of situation (Positive, Negative, and Neutral) and post-hoc paired t-test.
In ‘Stimulus assessment results’ of the Results section
Results from the assessment of the vividness, response intensity, and arousal of the
30 word stimuli are presented in Table 1. The vividness showed a significant result
in a main effect of parent (F1,23 = 7.63, p = 0.011), but not in a main effect of
situation (F2,46 = 0.46, p = 0.637) and an interaction effect (F2,46 = 1.08, p = 0.347).
In post-hoc analysis, the vividness was significantly greater in the mother condition
than in the father condition (t = 2.76, p = 0.011). The response intensity showed
significant results in a main effect of parent (F1,23 = 24.23, p < 0.001) and a main
effect of situation (F2,46 = 6.83, p = 0.003), but not in an interaction effect (F2,46
= 1.45, p = 0.246). Post-hoc analysis revealed that the response intensity was significantly
higher in the mother condition than in the father condition (t = 4.92, p < 0.001)
and significantly higher in the positive situation and negative condition than in
the neutral situation (t = 3.24, p = 0.004; t = 3.95, p = 0.001, respectively). The
arousal showed significant results in a main effect of parent (F1,23 = 6.66, p = 0.017)
and a main effect of situation (F2,46 = 5.62, p = 0.007), but not in an interaction
effect (F2,46 = 0.98, p = 0.384). In post-hoc analysis, the arousal was significantly
higher in the mother condition than in the father condition (t = 2.58, p = 0.017),
and in the positive and negative conditions than in the neutral condition (t = 3.35,
p = 0.003; t = 3.25, p = 0.004, respectively).
Reviewer #2:
Thank you very much for the possibility to review the manuscript titled "The neural
influence of autobiographical memory related to the parent-child relationship on psychological
health in adulthood". I think that this study contributes a lot to the literature
and should be published in this journal if the authors want to review some aspects
of the article that are lacking. This study investigates the neural influence on autobiographical
memories; however, the introductory section refers to several concepts not explored
in this work: emotional regulation, parent-child attachment. I think it may be important
to review the whole introductory section in order to better focus the present work.
In fact, the authors are invited to review studies related to the parent-child relationship
(rather than to the model of indivisual attachment) and to deepen the literature on
autobiographical memory.
For example, the authors are recommended to deepen their knowledge of the following
works, which would greatly enrich this manuscript:
Fivush, R., & Haden, C. A. (Eds.). (2003). Autobiographical memory and the construction
of a narrative self: Developmental and cultural perspectives. Psychology Press.
Fivush, R. et al. (1996). Remembering, recounting, and reminiscing: The development
of autobiographical memory in social context.
Cimino, S. et al. (2020). Dialogues about Emotional Events between Mothers with Anxiety,
Depression, Anorexia Nervosa, and No Diagnosis and Their Children. Parenting, 20(1),
69-82.
Reply:
We would like to express our gratitude for your optimistic evaluation of our research
and for drawing our attention to an important point. In the revised manuscript, descriptions
of emotion regulation and attachment were deleted because they were not directly related
to the research purpose. Instead, we added additional information to the introduction
to clarify autobiographical memory-related contents, including the references that
you suggested. Consequently, the introduction was entirely rewritten.
Revision:
In ‘the 1st to 3rd paragraphs’ of the Introduction section
Like the saying, “no health without mental health,” promoted by the WHO, psychological
health or psychological well-being is a fundamental factor contributing to quality
of life [1]. There are many factors that influence psychological health in adulthood,
and one of the most central determinants is the parent-child relationship [2]. The
relationship between a parent and child becomes the template for other interpersonal
relationships because attachment bonding allows a person to understand their environment
and establish a sense of security [3,4]. An examination of the association between
the retrospective perceptions of the parent-child relationship and emotional health
in adulthood showed that daily emotional and psychological distress are closely related
to how one perceives the quality of the parent-child relationship, and the retrospective
perceptions of father-child and mother-child relationships contribute to different
dimensions of emotional health [5]. Therefore, the perceptions of the childhood relationship
with parents are important in the overall well-being, even as adults.
The retrospective perceptions of the parent-child relationship are based on an individual’s
autobiographical memory. The development of autobiographical memory is a social process
that is influenced by the reminiscing style of parents, and thus an integral part
of the developing sense of self and interpersonal relatedness [6,7]. Autobiographical
memory represents the self and shapes emotional states of our everyday lives [8,9].
In general, memories are highly intertwined with features like self-referential processing
and emotion [9]. Functional neuroimaging studies have examined autobiographical memories
in reference to other types of memories. For instance, a recent study that compared
the difference between autobiographical memory and simple recognition memory found
that when a task required retrieval of life memories, default-mode areas were engaged
more, whereas a simple recollection of memories engaged the parietal memory network
[10]. Since autobiographical memory retrieval relies heavily on self-reference and
emotion, retrieval of autobiographical memories has been shown to employ various cortical
and subcortical regions, including the prefrontal and parietal cortices, anterior
cingulate cortex (ACC), precuneus, medial temporal cortex, hippocampus, and amygdala
[11-14]. In particular, the amygdala has been implicated in the encoding of emotional
memories [15] as well as retrieval of autobiographical memories [16]. Previous studies
also found coactivation of the amygdala, hippocampus, and inferior frontal gyrus (IFG)
during the retrieval of autobiographical memories [17] and neural responses in the
dorsal to caudal ACC and IFG elicited by the retrieval of painful autobiographical
memories [18]. These reports consistently show a close relationship between autobiographical
memory and emotional memory.
Psychological health is very closely related to memory encoding and retrieval, and
there is evidence supporting its influence on neural activities related to autobiographical
memory. Numerous studies have also shown the connection between psychological health
and selective memory bias. The representation, recall, and maintenance of autobiographical
memories have shown to be disturbed by individuals with poor psychological well-being,
where they are systematically biased for negative information [11]. Memory bias and
negative interpretations of events contribute to a vicious cycle, where one’s psychological
health contributes to the tendency toward negative interpretation of memories, and
this bias also maintains low self-esteem, depression, or anxiety [19-21]. In fact,
there is a consensus that self-esteem, anxiety, and depression are core elements of
psychological health [22-24]. The importance of these elements has spurred researchers
to study the close associations between self-esteem, anxiety and depression, and quality
of life in numerous fields [25-28].
Again with regard to the introductory section, the authors are invited to define more
clearly the objectives of the work and the hypotheses, consistent with the results
and discussions.
Reply:
As suggested, we revised the objective and hypothesis.
Revision:
In ‘the last paragraph’ of the Introduction section
In this study of the general population, we sought to identify the neural substrates
of the impression of parents while participants recalled childhood memories. For this
purpose, we examined how fathers and mothers are perceived differently and whether
the valence of memory influences this perception, and surveyed the effects of psychological
health (self-esteem, depression, and anxiety) on the memory process. As childhood
memories of parents triggered by various situations are inherently charged with emotions,
we hypothesized that regions often involved in an autobiographical memory, such as
the ACC, IFG, amygdala, and hippocampus, would be engaged differently depending on
the parent and the valence of situation, and would be modulated by a person’s psychological
health.
Discussions can also be reviewed in the light of the cited literature and authors
are invited to use an editing service for English language.
Reply:
As suggested, we have completely revised the discussion and the manuscript was reviewed
by a native speaker for English expression.
Revision:
In ‘the 1st to 8th paragraphs’ of the Discussion section
The present study examined the neural relationship between the perception of a parent
and the valence of an autobiographical memory, then explored how it is modulated by
one’s psychological health. We measured perception by inciting imagination of the
facial expression a parent had made in a given situation. The three seconds given
for the task may have been too short to remember an autobiographical memory. However,
since the vividness and reaction intensity in the stimulus assessments were rated
as moderately or higher, we can say that the task was to evoke an autobiographical
memory rather than an imagination or a simple impression. From our behavioral data,
we saw a rank in imagined emotion scores among the valences of childhood memories,
where positive situations elicited the highest imagined emotion score, followed by
neutral situations and negative situations. In conjunction with the RT results, we
could infer a sense of hesitation in choosing an appropriate expression especially
for negative childhood situations compared to positive situations.
The quality of communication between parents and children is an excellent indicator
of the quality of a parent-child relationship. Studies suggest that open communication
with parents allows children to learn skills that are closely related to healthy coping
skills and problem-solving strategies [54,55]. Thus, we assessed whether the quality
of the relationship with parents affects the impression of parents during childhood.
As expected, we found that more open communication with either father or mother was
correlated with a greater emotion score in positive emotion situations for both parents.
On the other hand, negative correlations were seen between communication problem scale
scores (father/mother) and the imagined emotion ratings for the respective parent-positive
conditions. Altogether, these findings convey that relationship quality directly affects
the recollection of one’s parents in positive contexts, but not necessarily in negative
situations. Moreover, the results also revealed that one’s level of self-esteem positively
influences the perception of one’s father, particularly in positive situations. This
finding further highlighted the influence of self-esteem on how positively one perceives
his or her father for positive memories, rather than rumination on exaggerated negative
affects seen in previous patient studies [19,41].
From the neuroimaging data, we saw intriguing neural responses to each condition from
the right caudal ACC and precuneus, in particular. In the result of the caudal ACC,
there was a particular bias toward father-negative and mother-positive, suggesting
that in the autobiographical memory of emotional events, different forms of brain
reactions occur depending on the parent's gender. Attention on the caudal ACC has
risen in recent years and studies have indicated that the region contributes significantly
to negative affect and pain processing [56-58]. This region receives an ample amount
of emotion-related and voluntary movement signals [59,60], and has been suggested
as a pivotal site for the emotional and voluntary interaction [58]. In a fascinating
investigation on pain processing in self and others, it was seen that the caudal ACC
was activated in response to self-experienced pain, but not when perceiving pain in
others [56]. Furthermore, this region was shown to increase in response to negatively
charged autobiographical memories [61]. On the other hand, its involvement in other-experienced
pain processing has also been reported. A meta-analysis on empathy-related regions
indicates that this region is part of the pain empathy network, and is engaged when
pain was anticipated [62]. Regardless, it is clear that the caudal ACC plays a role
in processing negative affect.
In light of these caudal ACC functions, our results may be linked to mothers taking
on the role of primary caretaker more so than the fathers. In many cultures, traditional
gender roles have determined the roles and expectations for parents, which usually
assumes fathers as breadwinners and mothers as the primary caretaker in child rearing
[63,64]. This point can be related to our results of the stimulus assessment. The
analysis of the stimulus assessments indicated that the responses that fathers gave
were less intense in all situations than those given by mothers; and the imagination
of fathers’ appearances were less vivid and evoked less arousal than that of the mothers.
In these respects, it is possible that caudal ACC activity may be a response to the
stoic and emotionally distant perception of fathers. Meanwhile, the importance of
memory to the mother can be seen in our result of negative correlation between caudal
ACC activity in the mother-positive condition and depression score. There was a report
that pathological changes in this region may be related to major depressive disorder
[65]. A study on the behavioral adaptation to unpleasant environment showed the involvement
of the caudal ACC to be critical in the ability to regulate the behavior [66]. It
has been suggested that the region might contribute to defending one from developing
depression [67]. Taken together, our result of the negative correlation in the mother-positive
condition may suggest that through the function of the caudal ACC, autobiographical
memories of positive events with the mother may act as a factor that prevents depression.
The precuneus, a central hub of the default mode network, also exhibited a similar
interaction effect between the parent and situation during the childhood memory recollection
task. The precuneus has been thought to play a critical role in episodic memory [68,69],
source monitoring [70], and self-referential processing [71]. Recently, a multivariate
analysis method, representational similarity analysis, demonstrated that the precuneus
is a key region engaged during the subjective experience of vivid autobiographical
memory reminiscence [72]. Other experiments have confirmed its prominent involvement
in the vividness of self-related memories [73,74]. In addition, right lateralization
of the precuneus has been shown for highly personal and vivid reminiscence of autobiographical
events [72]. Right lateralization is corroborated by the present study, which required
participants not only to visualize a given circumstance, but also to delineate the
facial expression by either parent. Our results indicate overall greater activation
of the right precuneus during recollection of fathers than mothers, and more specifically,
its activity was higher when recollecting fathers in negative compared to positive
situations. It is interesting to note that despite lower vividness score in the stimulus
assessments for fathers than mothers, these findings were observed, suggesting that
the perceptions of fathers may be more personal than those of mothers, especially
during reminiscence of negative situations. These may indicate the saliency of childhood
memories of fathers and particularly how fathers responded during negative circumstances.
In conjunction with activity of the caudal ACC, we cautiously conclude that memories
of fathers in negative situations have a more adverse effect as the negative impression
of fathers is more permanently embedded. This interpretation can also be linked to
the results of correlation with self-esteem.
Studies report that the neural structure of personal semantic memories serves as
a neural correlate of self-esteem [75,76]. It is postulated that due to its role in
using autobiographical memories to choose the applicable self-relevant information,
activation of the precuneus is closely related to self-esteem and how one processes
given information [76,77]. The current study confirmed the established association
between self-esteem and precuneus activity, as we found a negative relationship between
one’s self-esteem and precuneus activity during autobiographical reminiscence of fathers
in negative events. Recently, the precuneus was identified to correlate positively
with evaluation sensitivity, measured by a change in state self-esteem [75]. Together
with the evidence supporting the precuneus’ affiliation with evaluation sensitivity,
as well as the tendency for individuals with lower self-esteem to be more affected
by negative information [76], our result seems to suggest that the heightened activation
observed in individuals with lower self-esteem may be due to the saliency of negative
memories during recollection and their tendency to be more influenced by negative
information.
Our PPI analysis revealed significant increases in functional connectivity of the
caudal ACC with the fusiform gyrus and postcentral gyrus for the father-positive condition
compared to the mother-positive condition. Given that the fusiform gyrus processes
facial identity [78] and emotion [79], our finding may indicate that a greater sense
of negative affect was involved while processing facial expressions of fathers than
mothers in positive childhood events. This raises the possibility that the negative
affect arisen from processing emotional face expressions may be particularly different
between the parent in a positive context. Going back to the stimulus assessments,
we saw lower vividness, response intensity, and arousal from fathers than mothers.
Again, this may be since, generally, mothers are primary caregivers who spend more
time with children; thus, one may have more readily available positive memories involving
mothers than fathers to access on demand.
Previously, individuals with high trait anxiety have shown to hyperactivate the fusiform
gyrus while processing uncertain cues and angry faces [80,81]. Consistent with the
activation study, our study revealed that the connectivity strengths between the cingulate
cortex and fusiform gyrus during the father-positive versus mother-positive condition
correlated positively with the severity of anxiety symptoms. These results may provide
the neurobiological influence of trait anxiety in the retrieval of memory and the
perception of fathers. In addition to emotional face processing, greater connectivity
between the cingulate area and postcentral gyrus was witnessed for the father-positive
than mother-positive condition. Functional connectivity between these two regions
has been implicated in posttraumatic stress disorder (PTSD), where patients with PTSD
showed stronger connectivity than the control group, and also was positively correlated
with the severity of symptoms [82]. As part of the sensorimotor network [83], the
coupling of the caudal ACC and postcentral or paracentral gyri has been shown to be
involved in shock processing [84] and other emotional memory tasks [85]. Based on
the evidence, we postulate that the caudal ACC may relay negatively valenced affective
information to the sensorimotor area more for fathers than mothers when processing
facial expressions.
- Attachments
- Attachment
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