Master Thesis Child & Adolescent Psychology Date: 16-9-2019
Student number: s1516701 Supervisor: Elseline Hoekzema Second reader: Anne Miers
Pregnancy and the brain: a
study about changes in gray
matter volume and theory of
mind
Table of contents
Abstract ... 3
Introduction ... 4
Theory of mind ... 5
Social perception and the brain ... 7
Pregnancy and brain changes ... 8
The brain and social bonding ... 9
Hypotheses ... 10 Method ... 10 Participants ... 10 Final sample ... 11 Measures ... 12 Procedure ... 14 Statistics ... 15 Results ... 16 Discussion ... 20 References ... 22
Abstract
During pregnancy, the female body changes in many aspects. Does the brain change to prepare for caretaking as well? Studies suggest a decrease in gray matter (GM) volume in the brain due to pregnancy and show this decrease to be located mostly in brain areas underlying social perception. In our prospective study, we aimed to analyze GM changes in the superior temporal gyri of the brain and changes in a component of social perception, theory of mind (ToM), of women who experienced pregnancy (primiparous) compared to women who did not (nulliparous). Hereafter we analyzed whether these possible changes were correlated with each other. We predicted that GM volume would decrease and ToM ability would increase in women who experienced pregnancy. Furthermore, we predicted that these changes would be correlated with each other. Besides, we predicted that women who experienced pregnancy had an increased ToM ability for child stimuli. Measures included were the Reading the Mind in the Eyes Test (RMET) (ToM adult) and the Mind in the Child’s Eyes Test (MCET) (ToM child) and structural MRI in 36 primiparous women and 40 nulliparous women. Results demonstrate that the GM volume decreases significantly when comparing Pre and Post sessions in primiparous women compared to nulliparous women. No interaction effect was found between the Pre and Post sessions of the ToM tasks in both groups. Future research may provide further insight into the effects of pregnancy on the brain and changes in social perception due to pregnancy by brain studies and behavioral studies.
Keywords: Pregnancy, brain, superior temporal sulcus, superior temporal gyri, theory of mind, social perception
Introduction
Theory of mind (ToM) is defined as the ability to understand and explain other people's mental state (Gallagher & Frith, 2003). It is popularly referred to as the ability to empathize with others. In short, it makes it possible for us to reflect on our own and other people's thoughts (Baron-Cohen, 2001). This ability to reflect ensures that we are able to work together more efficiently or, on the contrary, know how to estimate danger more efficiently, which increases the chance of our survival (Gallagher & Frith, 2003).
Many changes occur during pregnancy, both in the body and in the brain. The body of women changes and prepares for the development of the child and giving birth. It would be logical for the brain to do this as well, but not much is known about this yet. There are a few points that are relevant for possible changes of the pregnant brain. First, it would be important for the mother to be prepared to assess the needs of the child. For example, being able to recognize when the child is hungry or thirsty, or when it needs a hug (Baron-Cohen, 1999).
Second, it would also be important to know how to teach a child, according to
Baron-Cohen (1999). An essential quality of a mother is the ability to empathize with the level of knowledge of the child, also known as the tracking of mental states (Csibra & Gergely, 2006). This is necessary in order to be able to gradually teach the child until it is able to do
something alone. The child learns not only through observation but also through a shared intention between parent and child to do something with the object of choice (Senju & Csibra, 2008).
At last, a dangerous situation may occur and the mother may be forced to protect the child. The mother needs the ability to estimate the level of danger and hence determine efficiently what she will do to secure the child (Gallagher & Frith, 2003).
These three roles the ToM plays after giving birth could increase the child's chance of survival. Therefore, the ability to understand and estimate other people's mental state serves
as an evolutionary biological benefit for mothers. The first results of investigations in this area are promising, but still little is known about the effect of pregnancy on the brain. This research will provide new insights that will be useful in scientifically mapping changes in the female brain.
In this study we will investigate whether the ToM of women who have been pregnant has changed due to pregnancy and whether this can also be seen as a change in a specific area of the brain, as a change in the gray matter (GM) volume of the superior temporal gyri (a part of the STS). This will be investigated through a prospective study (before and after
pregnancy) which includes primiparous (first time) mothers and nulliparous women for control.
In the following content, results of investigations about ToM will be discussed.
Hereafter, results of investigations about the brain in relation to ToM will be discussed.
Theory of mind
To understand and explain the mental state of others (ToM), the model of Shamay-Tsoory et al. (2010) suggests two forms of ToM to be distinguished. The first form is the cognitive form, which refers to the ability to make inferences about beliefs and motivations. The second form is called the affective form, which refers to the ability to infer what another individual is feeling. Shamay-Tsoory et al. (2010) believe that cognitive ToM is a prerequisite for affective ToM because this last form requires intact empathy processing. They suggest that integrating the two forms of ToM would provide a successful affective ToM processing.
Our research will focus on the prerequisite (cognitive) ToM form. To infer about beliefs and motivations, it is necessary to understand and recognize non-verbal cues (Hall & Bernieri, 2001; Knapp & Hall, 1997), such as differences on faces, voice perception or biological movements and linguistic processing (Deen, Koldewyn, Kanwisher, & Saxe, 2015;
Riggio, 1992). According to Baron-Cohen (2001), the perception about emotions on faces could be investigated by choosing the most applicable emotion when seeing a pair of eyes.
The basic emotions are, according to Ekman and Friesen (1971) and Walker (1982), happiness, sadness, anger, fear and disgust. These basic emotions have been chosen because they are recognized by all cultures as pure emotions. In this sense pure emotions are emotions in which no cognitive attribution needs to be assigned to the person concerned. Also, because they are recognized even by very young normally developed children (Ekman & Friesen, 1971; Walker, 1982). According to Baron-Cohen (2001), more complex emotions (such as surprise or confusion) require a higher effort to estimate the other person's mental state (ToM) and thus form a more reliable test battery than pure emotions.
Women have a greater ability to understand these emotional expressions than men and the development of this ability already starts in infancy (Rosip & Hall, 2004). Additional findings provide an indication for a gender difference in favor of women in both infancy and child trials (McClure, 2000). These results may indicate a biological benefit that women need to protect and nurture a child. Furthermore, there are preliminary indications for social
information to be processed more quickly by pregnant women, including an increase in emotion recognition and face recognition (Anderson & Rutherford, 2011; Anderson & Rutherford, 2012).
Taken together, these findings argue the different forms of ToM, and the necessary role of the recognition of emotions on faces (in our case, in the eyes). Furthermore, the comment of Baron-Cohen (2001) argues the importance of using complex emotions when testing ToM. Moreover, the findings suggest a benefit in favor of women to recognize and understand the emotional expressions. Furthermore, there are preliminary indications for social information to be processed more quickly by pregnant women which could indicate a change in the female brain due to pregnancy.
Social perception and the brain
Zilbovicius et al. (2006) argue that social perception is defined as a combination of eye-gaze processing, recognizing someone else's pointing gestures, and hereafter processing and using this information to understand and explain other people's mental state (ToM).
Social information processing is carried out through a combination of different brain areas and networks. For example, the fusiform gyri are linked to the processing of invariant aspects of faces (Kanwisher et al., 1997; Roisson et al., 2003; Ishai et al., 2005) and bodies (Peelen & Downing, 2007). A relationship has also been found between the temporo-occipital extrastriate body area and the processing of bodies (Peelen & Downing, 2007). Furthermore, a link has been found for a central role of the amygdala in the processing of emotional signals such as facial expressions (Breiter et al., 1996; Morris et al., 1996). Furthermore, Schurz et al. (2014) meta-analyzed imaging studies on ToM and found overlap in brain activation for the medial prefrontal cortex (mPFC) and the bilateral posterior temporo- parietal junction (TPJ). In addition, they found task-related differences in activity in the areas surrounding the mPFC and bilateral TPJ. Among others, the precuneus, temporal lobes and inferior frontal gyri had profiles of task-related activation. Moreover, the putative "mirror-neuron system" in parts of the parietal and premotor cortices (Rizzolatti & Craighero, 2004) is associated with
understanding other people's goal-directed actions. Haxby et al. (2000) found the inferior occipital gyri, the lateral fusiform gyrus and the superior temporal sulcus to be the core of the human system of face perception. The lateral fusiform gyrus would be involved in the
representation of identity of faces, the superior temporal sulcus would be involved in the changeable aspects of faces. The inferior occipital gyri would provide input in both the lateral fusiform gyrus and superior temporal sulcus.
Lahnakoski et al. (2012) found that the superior temporal sulcus (STS) responded to all 8 tested social features through an fMRI study (emotions being one of them), where the other brain regions showed a more narrowly tuned response profile to specific social features
such as emotions. The STS is one of the longest sulci in the brain, extending from the inferior paretal lobe anteriorly along the full length of the temporal lobe. Deen, Koldewyn, Kanwisher and Saxe (2015) found that the region posterior STS and regions nearby like the superior temporal gyri responded specifically to ToM, but also to faces, voice perception of biological movements and linguistic processing.
Summarizing, these findings suggest a network of brain areas to be responsible for social perception, and more specifically, ToM. Moreover, there are findings which suggest a role for the STS area in social perception, among which perception about faces.
Pregnancy and brain changes
There have been few studies investigating the effect of pregnancy on the brain. During
pregnancy, changes are seen in the brain. There are speculations about the role hormones play in these changes. For example, an increase in progesterone and estrogen is known to happen due to pregnancy (Casey, MacDonald, Sargent, & Starkey, 1993). These sex hormones serve as regulators for morphological neuronal changes in the brain (Simerly, 2002). Carmona et al. (2019) found an association between brain changes in adolescence and pregnancy and found a decrease in GM volume in adolescence. These findings suggest that GM volume decreases when sex steroid hormonal changes occur.
Hoekzema et al. (2017), investigated the effects of pregnancy on the brain and found changes in the brain in areas underlying ToM. A decrease in GM volume was found in the posterior midline, the bilateral lateral prefrontal cortex and the bilateral temporal cortex. Additionally, the greatest overlap with GM changes of pregnancy was found for the cognitive components underlying ToM, and the greatest spatial correspondence was found with the network of strongest ToM recruitment.
Additionally, people with autism spectrum disorder (ASD) who have more difficulty with social perception often have more trouble with joint attention, empathizing and
understanding others (Zilbovicius et al., 2006). Several brain-imaging studies have found an indication for an above average GM volume in the STS brain area while investigating people with ASD (Boddaert et al., 2004).
Collectively, these results suggest a change in the female brain, driven by hormone changes due to pregnancy, in the GM volume of brain areas underlying ToM.
The brain and social bonding
Seeing faces of close friends and family compared to people with whom you have no personal relationship, such as celebrities, causes areas of the brain to produce neural responses
(Gobbini et al., In press). The areas responsible for delivering these neural responses are mediators of emotional responses such as episodic memory and areas dealing with the mental state of others (ToM). In particular with close relatives, activations are found in the posterior cingulate-precuneus region, the superior temporal sulcus (STS) and the anterior paracingulate (Gobbini et al., In Press).
Bartels and Zeki (2000) ague the importance of a balance between activation and deactivation, since the nature and strength of an emotion may be dictated by a complex balance between the two. They found a decrease in activity when viewing pictures of a loved partner in foci in the medial insula and the anterior cingulate cortex. At subcortical level, they found a decrease in the posterior cingulate gyrus and in the amygdala.
These findings suggest that a network of areas is responsible for an affective state. Additionally, Swain et al. (2007) argue that this neural network may have an underlying function in the parent-infant attachment and has an overlap with other forms of social bonding such as with romantic love. This would therefore indicate that this network of areas is
responsible for an emotional response. Moreover, Hoekzema et al. (2017) found that reductions in GM volume could predict increases in maternal attachment.
We hereby discuss that women who experienced pregnancy might estimate the state of mind more of children more efficiently, because they have an emotional bond with their own child, than the state of mind of adults. In contrast, another possibility would be a general increase in ToM ability in order to recognize social cues signaling danger as a mother.
Hypotheses
We expect that becoming a mother will increase the ToM ability and that this ability is more pronounced when it comes to processing stimuli from children than from adults. We predict a difference in the changes between sessions on the ToM task, which will show that
primiparous women will perform with greater accuracy than nulliparous women. Moreover, we expect a difference in the changes between sessions in GM volume, which will show a decrease in GM volume for primiparous women. Additionally, we expect that ToM ability is negatively correlated to GM volume in the superior temporal gyri.
Method Participants
For this prospective cohort study, first-time mothers participated in an MRI acquisition before and after their pregnancy, allowing us to use each woman's pre-pregnancy brain scan as her individual baseline. Data were collected over a total period of approximately 4 years.
We sought nulliparous individuals who were planning to try to become pregnant in the near future but were not pregnant yet and nulliparous individuals without such plans. Participants were therefore not randomly assigned to groups. Recruitment and data collection for all groups was initiated at the same time. Although individuals were
recruited separately for the pregnancy (EXP1) groups (women becoming a parent between the sessions) and the control (CTR) groups (women who did not become pregnant within this time frame) on the basis of their intention to become a parent in the near future, the
final group allocation depended on the transition from nulliparity into primiparity in between sessions.
Women trying to become pregnant were scanned in the early follicular phase of their menstrual cycle or before the insemination or transfer in the fertility-treated group. Only participants who had never experienced a previous pregnancy beyond the first trimester were included in the study. The main criterion for continuing in the study for participants in the EXP1 group was achieving pregnancy in the period following the first MRI session.
Final sample
Our final sample consisted of the following subject groups with complete (MRI and RMET/MCET) Pre and Post data sets: 25 primiparous women (EXP1), 36 nulliparous control women (CTR). Besides this complete group, a group with only RMET/MCET Pre and Post data was analyzed. The following subject groups were included: 36 primiparous women, 40 nulliparous control women.
Group A (MRI and RMET/MCET)
The average age of group A was 29, in both the EXP1 group and CTR group. The educational level according to Verhage (1964) was for the EXP1 group: 1 participant graduated lower than expended lower education (MULO, code 4), 3 participants graduated MULO (code 5), 7 participants graduated secondary higher education such as HAVO and VWO or higher professional education such as HBO (VMHO, code 6) and 14 participants graduated university (WO, code 7). For the CTR group the educational level was: 1 participant MULO, 10 participants VMHO and 25 participants WO. The Post session took place on average at 416 days for the EXP1 group and at 430 days for the CTR group after the Pre session.
The average age of group B was 29 as well, in both the EXP1 group and CTR group. The educational level was for the EXP1 group: 1 participant lower than MULO, 3 participants MULO, 11 participants VMHO, and 21 participants WO. For the CTR group the
educational level was: 1 participant MULO, 12 participants VMHO and 27 participants WO. The Post session took place on average at 470 days for the EXP1 group and at 432 days for the CTR group after the Pre session.
Measures MRI
The GM volume is measured in the STS area (gyri) by means of MRI-images in a Philips 3T scanner. High-resolution anatomical MRI brain scans were acquired using a
T1-weighted gradient echo pulse sequence (TR = 8.2 ms, TE = 3.7 ms, NSA = 1, matrix = 256 × 256, FOV = 240 mm, 180 slices, thickness = 1 mm, no gap, FA 8 °). To investigate the structural changes in the GM volume, a surface-based analysis was performed in
FreeSurfer 5.3. In this research we could make use of data that was processed by means of
the longitudinal stream in FreeSurfer to extract regional brain volumes.The approach of the
FreeSurfer 5.3 is explained in the paper of Hoekzema et al. (2017). RMET and MCET
To test the ability to understand and explain the mental state of another person (ToM) we used the RMET (Baron-Cohen, 2001) and the MCET (Duff & Schulte-Mecklenbeck, 2010). These tests require an understanding and recognizing of the more complex emotions. However, it is important to note, according to Baron-Cohen (2001), that the RMET only tests the first form of ToM (cognitive) and not the second (affective). Baron-Cohen does argue the importance of the cognitive form of ToM and thinks the RMET is an important first step to be able to measure ToM.
The participants performed the RMET and MCET while they were in the MRI scanner. Before the test started, they were shown a similar explanation about the tests on the screen in the scanner. After this, the researcher first started the RMET and then the MCET. The participants were not given feedback about their performance after the Pre session, hence this could not interfere in the task or relate to personal characteristics about
wanting to perform well or competitiveness. The fMRI data obtained from these tasks is
not part of this thesis.
Participants were firstly shown glances from adults in this task. When they saw the word “EMOTION”, a number of photos followed with 2 words below that give a possible description of what this person thinks or feels. Participants were asked to choose the word that best describes what the person thinks or feels. When they found both words applicable, they still chose the word they considered most suitable.
Two examples from the RMET (left) and MCET (right):
Panic hatred confused surprised
As a control task for the fMRI task, the test included questions about gender. When participants saw the word "SEX", a number of photos followed with the words "male" or "female" below. If the participant thought that the gaze was of a man, "male" was chosen and if the participant thought it was a woman, "female" was chosen. When in doubt, it was recommended to choose the first answer that came to mind.
The Mind in a Child's Eyes task (MCET) tests the ToM skill when seeing the looks of children. The test has the same procedure as the RMET. Responses could be given in both the
RMET and the MCET through a button box that was held in the right hand while scanning in the MRI. The participants only used the leftmost buttons for the task. The participants were given 5 seconds per photo to answer. Participants received 1 point per correct answer. Participants could obtain a total of 36 points per task if they had correctly assessed all the views.
See the button box below:
Procedure
Participants were recruited by word of mouth and flyers. When the requirements for participating in the investigation were met, an appointment was made for the first session (Pre). Participants had to communicate with the researchers when they were ready for the Post session. Before both sessions (Pre and Post), participants had to fill in an informed consent. When participants arrived at the Leids Universiteit Medisch Centrum (LUMC), they were accompanied by a researcher to the MRI area of the LUMC. Before going into the MRI room, participants were controlled for any metal and had to change into MRI clothes. Herafter, participants entered the MRI room and layed down in the scanner. Participants had to perform several cognitive tests (one of them being the ToM task) and could watch a Netflix series or film in between tests. In total participants layed in the scanner for approximately 2 hours. After participation, the payment as pre-arranged was given.
Statistics
To investigate whether there is an association between the brain changes of pregnancy and changes in ToM ability, we investigated changes in the GM volume across pregnancy in relation to ToM. A repeated measures ANOVA analysis was conducted to analyze whether a group difference was found between Pre and Post sessions. When a significant interaction effect was found between group and session, a paired sampled t-test was used to investigate whether this effect occurred due to a significant change in the EXP1 group and that this effect therefore could be an indication for an effect of pregnancy.
For both group A and group B, the within-subjects factor was time (Pre, Post). For the GM volume in the superior temporal gyri two levels were included: Volume GM Pre and Volume GM Post). For the ToM ability also two levels were included: ToM child and ToM adult (Variable names: ToM child Pre, Tom child Post and ToM adult Pre, ToM adult Post). The between-subjects factor for group 1 was the difference in group (EXP1 or CTR). For group B, only the ToM factor, as mentioned above, was used.
For only group A, a correlation analysis was conducted, when there were significant differences in both GM volume and ToM ability, to identify whether there was a correlation between the possible change in GM volume and ToM ability.
Before running the repeated measures ANOVA analysis, assumptions were analyzed. These assumptions were normality and sphericity. For testing the normality, a histogram for every within-subjects factor was produced and the Shapiro-Wilk test was used. The
assumption for normality was met. In this research, Mauchly’s test was not necessary because there were only two sessions. Furthermore, outliers were investigated. For Pre and Post GM volume variables, there was one outlier. When analyzing without this outlier, no differences in results were seen. For the Pre ToM variables (both child and adult) and the Post ToM adult variable, there were no outliers. For the Post ToM child variable, two outliers were found. No differences in results were seen when analyzing without these outliers.
Results
In addition to the averages and standard deviations of the demographic data, Table 1 also contains a group comparison of the demographic data computed by an independent sample t-test. The group comparison displays no significant differences between the two groups (EXP1 and CTR) in terms of demographic data. In Table 2, the means and standard deviations of all variables are displayed.
Table 1. Demographics and statistics of group A and group B.
EXP1 M(SD) CTR M(SD) t p Age group A 29.44(3.61) 29.08(3.48) .34 .70 Ed. Level group A 6.36(0.86) 6.66(0.53) -1.72 .09 Time between Pre and Post
group A 416.16(81.96) 430.36(87.96) -.64 .53 Age group B 29.06(3.36) 29.33(3.57) -.34 .74 Ed. Level group B 6.44(0.77) 6.65(0.53) -1.36 .18
Time between Pre and Post
group B
469.53(119.12) 431.70(89.57) 1.57 .12
Table 2. Means and standard deviations of the variables for the RMET: ToM child stimuli, ToM adult stimuli, and for the MRI data: volume in GM. For all variables Pre and Post sessions were included.
Groups N M SD
EXP1
ToM child Pre 36 22.0278 1.90467
ToM adult Pre 36 25.0278 2.15786
ToM child Post 36 22.1389 2.23163
ToM adult Post 36 25.0000 2.50713
Vol GM Pre 25 16537.44 1673.68
Vol GM Post 25 16244.46 1639.29
CTR
ToM child Pre 40 22.1000 1.87835
ToM adult Pre 40 24.8000 1.88380
ToM child Post 40 21.7000 2.44110
ToM adult Post 40 25.6750 2.20009
Volume GM Pre 36 16587.64 1618.88
Volume GM
Post 36 16698.17 1589.91
A significant interaction effect was found between group and session for the GM volume when conducting the repeated measures ANOVA, F(1, 59) = 21.307, p < .001. Hereafter a paired sampled t-test was conducted in EXP1 and CTR to investigate whether
these changes occur due to significant changes in the EXP1 group. A significant change was found (decrease in GM volume) for the EXP1 group: t(24) = 4.254, p = .00. No significant change was found for the CTR group: t(35) = -2.011, p = .052. Figure 1 represents the results.
Figure 1. Comparison of the mean and SEM of GM volume of Pre and Post sessions for the experimental (EXP1) and the control (CTR) group.
The repeated measures ANOVA for ToM ability showed no interaction effects between the group and the session, for ToM child: F(1, 74): .842, p = .362, and for ToM adult: F(1, 74) = 2.08, p = .153. The repeated measures ANOVA ToM results are displayed in Figure 2 and 3.
Figure 2. Comparison of the mean and SEM of ToM ability for child stimuli of Pre and Post sessions, for the experimental (EXP1) and control (CTR) group.
Figure 3. Figure 2. Comparison of the mean and SEM for ToM ability for adult stimuli of Pre and Post sessions, for the experimental (EXP1) and control (CTR) group.
Because there were no significant differences between the ToM Pre and Post variables, no further correlation analyses were conducted with the GM volume.
Discussion
As expected by the results of the investigations of Hoekzema et al. (2017) and Boddaert et al. (2004), we found a significant interaction effect between group and session in terms of a decrease in GM volume. This decrease only appeared for the EXP1 group and not for the CTR group which confirms the theory of a decrease in de GM volume due to pregnancy. Results of investigations of Hoekzema et al. (2017) imply that reductions in GM volume could estimate increases in maternal attachment. Furthermore, Carmona et al. (2019) found an association between brain changes in adolescence and pregnancy and found a decrease in GM volume in adolescence. These findings, combined with our findings, suggest that GM volume decreases when sex steroid hormonal changes occur. Functions of the superior temporal gyrus are auditory processing, including language, biological movement and other aspects of social cognition (Deen, Koldewyn, Kanwisher and Saxe, 2015), which could indicate that the decrease in GM volume found in the superior temporal gyri could contribute to social perception. It is important to take into account that we did not scan during pregnancy itself, and that the hormone values were not yet available. Therefore, we can not be sure whether the decrease in GM volume we found, is an effect due to pregnancy or a postpartum effect.
When comparing the ToM child and ToM adult variables, we found no
association between pregnancy and ToM ability. Hence, both emotion child and adult stimuli were not more efficiently recognized by primiparous women (EXP1) compared to nulliparous women (CTR). Moreover, in contrast to findings of Gobbini et al. (In press), we found that primiparous women did not have an enhanced ability to estimate the mental state of children. Important to take into account is the comment of Baron-Cohen (2001) when observing the RMET. He argued that the RMET only tests the cognitive form of ToM and not the affective
form. Furthermore, Kurke et al. (2018) found through testing the reliability of several theory of mind paradigms that they seem less reliable and valid than previously assumed, and therefore limiting the conclusions that could be drawn from these kinds of tests.
For the comment of Baron-Cohen (2001), additional tests, covering the ability to infer what another person is feeling, could provide a complete image of the ToM ability. For example, the “Strange Stories Test” (Happé, 1994) could provide a more pronounced image of the ToM ability. This test includes 16 stories followed by questions and investigates
whether participants understand the characters’ feelings and thoughts. A second ToM test that could provide a more complete image of the ToM ability is the “Faux Pas Test” (Stone et al., 1998). This test examines the ability to identify whether something inappropriate has been said (which may hurt another’s feelings). For future research in the brain, it would be important to focus on the superior temporal sulcus instead of the superior temporal gyri. Another possibility for future research would be to include hormones, in order to examine whether there is an association between hormone changes and ToM. Additionally, future studies could examine the effect of maternal attachment on estimating the mental state of children in primiparous women compared to nulliparous women.
Coming back to the investigation of Hoekzema et al. (2017), this investigation gives us important insights in the association between pregnancy and the brain. In order to analyze whether changes in a brain area related to ToM are related to changes in ToM due to pregnancy, this investigation was conducted. Taken together, this research provided important additional results for a decrease in GM volume in the STS area (gyri). Future investigations will be necessary to focus on the sulcus instead of the gyri, to investigate the effect of hormones and to investigate ToM including the affective form. For now, this investigation provides strong additional information about changes in the female brain due to pregnancy.
References
Anderson, M. V., & Rutherford, M. D. (2011). Recognition of novel faces after single exposure is enhanced during pregnancy. Evol. Psychol., 9, 47-60.
Anderson, M. V., & Rutherford, M. D. (2012). Cognitive reorganization during pregnancy and the postpartum period: an evolutionary perspective. Evol. Psychol., 10, 659-687.
Bartels, A., & Zeki, S. (2000). The neural basis of romantic love. NeuroReport, 11(17), 3829- 3834. Baron-Cohen, S. (2001). Theory of Mind in normal development and autism. Prisme, 34, 174-183. Baron-Cohen, S. (1999). Evolution of a theory of mind? In Corbalis, M., & Lea, S. (eds). The
descent of mind: psychological perspectives on hominid evolution. Oxford University Press 1999.
Baron-Cohen, S., Ring, H., Moriarty, J., Schmitz, B., Costa, D., & Ell, P. (1994). Recognition of mental state terms. Clinical findings in children with autism and a functional neuroimaging study of normal adults. Br. J. Psychiatry,165, 640–649.
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., Plumb, I. (2001). The “Reading the Mind in the Eyes” Test Revised Version: A Study with Normal Adults with Asperger Syndrome or Higher-functioning Autism. J. Child Psychol. Psychiat., 42(2), 241-251.
Boddaert, N., Chabane, N., Gervais, H., Good, C. D., Bourgeois, M., Plumet, M. H., Barthélémy, C., Mouren, M. C., Artiges, E., Samson, Y., Brunelle, F., Frackowiak, R. S., & Zilbovicius, M. (2004). Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. NeuroImage, 23, 364–369.
Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, C. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996). Response and habituation of the human
amygdala during visual processing of facial expression. Neuron, 17, 875–887. Carmona, S., Martínez-García, M., Paternina-Die, M., Barbra-Müller, E., Wierenga, L. M.,
Picado, M., Lucco, F., García-García, D., Soliva, J. C., Tobeña, A., Peper, J. S., Crone, E. A., Ballesteros, A., Vilarroya, O., Desco, M., Hoekzema, E. (2019). Pregnancy and adolescence entail similar neuroanatomical adaptations: A comparative analysis of cerebral morphometric changes. Hum. Brain Mapp, 40, 2143-2152.
Csibra, G., & Gergely, G. (2006). Social learning and social cognition: the case for pedagogy. In Processes of Change in Brain and Cognitive Development. Attention and Performance XXI, ed. Y Munakata, MH Johnson, pp. 249-74. Oxford, UK: Oxford Univ. Press Identifies pedagogy as a crucial process in human social cognition.
Deen, B., Koldewyn, K., Kanwisher, N., & Saxe, R. (2015). Functional Organization of Social Perception and Cognition in the superior Temporal Sulcus. Cerebral Cortex, 25, 4596-4609. Duff, S. C., & Schulte-Mecklenbeck, M. (2010). The mind in a child’s eyes: A test of theory of mind
skills with child stimuli. In press.
Ekman, P., & Friesen, W. (1971). Constants across cultures in the face and emotion. Journal of Personality and Social Psychology, 17, 124–129.
Frith, C. D., & Frith, U. (1999). Interacting minds – a biological basis. Science, 286, 1692–1695. Gallagher, H. L., & Frith, C. D. (2003). Functional imaging of ‘theory of mind’. Cognitive Science,
7(2), 77-83.
Gobbini, M. I., Leibenluft, E., Santiago, N., & Haxby, J. V. (in press): Social and emotional attachment in the neural representation of faces. Neuro Image.
Hall, J. A., & Bernieri, F. J. (Eds.), (2001). Interpersonal sensitivity: Theory and measurement. Hillsdale, NJ: Erlbaum.
Happé, F. (1994). An advanced test of theory of mind: Understanding of story characters thoughts and feelings by able autistic, mentally handicapped and normal children and adults. Journal of Autism and Developmental Disorders, 24, 129–154.
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223–233.
Hoekzema, E., Barba-Müller, E., Pozzobon, C., Picado, M., Lucco, F., García-García, D., Carlos Soliva, J., Tobeña, A., Desco, M., A Crone, E., Ballesteros, A., Carmona, S., & Vilarroy, O. (2017). Pregnancy leads to long-lasting changes in human brain structure. Nature
neuroscience, 20(2), 287-300.
Ishai, A., Schmidt, C. F., & Boesinger, P. (2005). Face perception is mediated by a distributed cortical network. Brain Res. Bull. 67, 87–93.
Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311.
Knapp, M. L., & Hall, J. A. (1997). Nonverbal communication in human interaction (4th ed.), Belmont, CA: Wadsworth, Thompson Learning.
Kurke, L., Duhn, B., Schneider, D., Rakoczy, H. (2018). Is Implicit Theory of Mind a Real and Robust Phenomenon? Results From a Systematic Replication Study. Psychological Science, 29(6), 888-900.
Lahnakoski, J. M., Glerean, E., Salmi, J., Jääskeläinen, I. P., Sams, M., Hari, R., & Nummenmaa, L. (2012). Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception. Front Hum Neurosci, 6, 233.
McClure, E. B. (2000). Meta-analytic review of sex differences in facial expression processing and their development in infants, children and adolescents. Psychological Bulletin, 126(3), 424-453. doi:10.1037/0033- 2909.126.3.424
Morris, J. S., Frith, C. D., Perret, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996). A differential neural response in the human amygdala to fearful and happyfacial expressions. Nature, 383, 812–815.
Peelen, M. V., & Downing, P. E. (2007). The neural basis of visual body perception. Nat. Rev. Neurosci. 8, 636–648.
Rosip, J. C., & Hall, J. A. (2004). Knowledge of nonverbal cues, gender, and nonverbal decoding accuracy. Journal of Nonverbal Behavior, 28(4), 276- 286. doi:10.1007/s10919-004-4159-6 Rossion, B., Caldara, R., Seghier, M., Schuller, A. M., Lazeyras, F., & Mayer, E. (2003). A network
of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126, 2381–2395.
Riggio, R. E. (1992). Social interaction skills and nonverbal behavior. In R. S. Feldman (Ed.), Applications of nonverbal behavioral theories and research, (pp. 3-30). HiUsdale, NJ: Erlbaum.
Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169– 192.
Schurz, M., Radua, J., Aichhorn, M., Richlan, F., Perner, J. (2014). Fractionating theory of mind: A meta-analysis of functional brain imaging studies. Neuroscience and Biobehavioral Reviews, 42, 9-34.
Shamay-Tsoory, S. G., Harari, H., Aharon-Peretz, J., Levkovitz, Y. (2010). The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies. Cortex, 46(5), 668–77.
Senju, A., & Csibra, G. (2008). Gaze following in human infants depends on communicative signals. Curr. Biol., 18, 668-71.
Stone, V. E., Baron-Cohen, S., & Knight, R. T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10, 640–656.
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007). Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry, 48, 262-287.
Verhage, F. (1964). Intelligentie en leeftijd: Onderzoek bij Nederlanders van twaalf tot zevenenzeventig jaar. Assen: Van Gorcum.
Walker, A. S. (1982). Intermodal perception of expressive behaviours by human infants. Journal of Experimental Child Psychology, 33, 514–535.
Zilbovicius, M., Meresse1, I., Chabane, N., Brunelle, F., Samson, Y., & Boddaert, N. (2006). Autism, the superior temporal sulcus and social perception. TRENDS in Neurosciences, 29(7), 359-366.
