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Attachment style dimensions are associated with brain activity in response to gaze interaction a

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Marco Cecchini , Maria Elena Iannoni , Anna Lucia Pandolfo , Paola Aceto & Carlo Lai a

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Department of Dynamic and Clinical Psychology, Sapienza University, Rome, Italy

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Department of Anaesthesiology and Intensive Care, Catholic University of Sacred Heart, Rome, Italy Published online: 08 Jan 2015.

Click for updates To cite this article: Marco Cecchini, Maria Elena Iannoni, Anna Lucia Pandolfo, Paola Aceto & Carlo Lai (2015): Attachment style dimensions are associated with brain activity in response to gaze interaction, Social Neuroscience, DOI: 10.1080/17470919.2014.998344 To link to this article: http://dx.doi.org/10.1080/17470919.2014.998344

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SOCIAL NEUROSCIENCE, 2015 http://dx.doi.org/10.1080/17470919.2014.998344

Attachment style dimensions are associated with brain activity in response to gaze interaction Marco Cecchini1, Maria Elena Iannoni1, Anna Lucia Pandolfo1, Paola Aceto2, and Carlo Lai1 1

Department of Dynamic and Clinical Psychology, Sapienza University, Rome, Italy Department of Anaesthesiology and Intensive Care, Catholic University of Sacred Heart, Rome, Italy

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Aim of the present study was to investigate the time course of brain processes involved in the visual perception of different gaze interactions in woman–child dyads and the association between attachment dimensions and brain activation during the presentation of gaze interactions. The hypothesis was that the woman avoidance will produce a greater activation of primary somatosensory and limbic areas. The attachment styles dimensions avoidant-related will be associated with fronto-limbic brain intensity during the convergence of gaze. Electroencephalogram (EEG) data were recorded using a 256-channel HydroCel Geodesic Sensor Net in 44 female subjects (age: 24 ± 2 years). Event-related potential (ERP) components and standardized low-resolution electromagnetic tomography (sLORETA) were analyzed. Participants were administered the attachment style questionnaire before EEG task. A lower P350 latency was found in the fronto-central montage in response to woman avoidance. sLORETA analysis showed a greater intensity of limbic and primary somatosensory areas in response to woman avoidance compared to the others gaze interactions. In response to convergence gaze, the confidence attachment dimension was negatively correlated with the intensities of the right temporal and limbic areas, and the relationships as secondary attachment dimension were positively correlated with the intensities of the bilateral frontal areas and of the left parietal area.

Keywords: Gaze interactions; Neural correlates; ERPs; sLORETA; Adult attachment dimensions.

Over the past 20 years, the great scientific interest with respect to how humans perceive and process the face of human beings has been investigated by measuring brain activity (Bentin, Allison, Puce, Perez, & McCarthy, 1996; Bötzel, Schulze, & Stodieck, 1995; Carmel & Bentin, 2002; de Haan, Pascalis, & Johnson, 2002; Eimer, 2000a; Itier & Taylor, 2002, 2004a, 2004b; Linkenkaer-Hansen et al., 1998; Macchi Cassia, Westerlund, Kuefner, & Nelson, 2006; McPartland, Cheung, Perszyk, & Mayes, 2010; Rossion, Delvenne, et al., 1999; Rossion et al., 2000, 2003; Rousselet, Mace, & FabreThorpe, 2004; Sagiv & Bentin, 2001). These studies have highlighted the important role played by the eyes and gaze direction in the social and

nonverbal communication. The human eye has the greatest amount of visible sclera compared to other animal species, and this allows to clearly distinguish the gaze direction of others even at distance (Kobayashi & Kohshima, 1997, 2001). This morphological feature provides a great advantage for survival, and it gives at the eyes and gaze direction an important role in social cognition (Cecchini, Aceto, Altavilla, Palumbo, & Lai, 2013). Mutual gaze is crucial in the establishing interpersonal relationships from the birth (Cecchini et al., 2007, 2010; Cecchini, Baroni, et al., 2013). Most of the event-related potential (ERP) studies that have investigated the processing of the human eyes and the gaze direction focused primarily on the

Correspondence should be addressed to: Carlo Lai, Department of Dynamic and Clinical Psychology, Sapienza University of Rome, Via degli Apuli 1, 00185, Roma, Italy. E-mail: [email protected]

© 2015 Taylor & Francis

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early components of the ERP signal (Bentin et al., 1996, 2007; Itier, Latinus, & Taylor, 2006; Jemel, George, Chaby, Fiori, & Renault, 1999; Klucharev & Sams, 2004; McPartland et al., 2010; Righart, Burra, & Vuilleumier, 2011; Schweinberger, Kloth, & Jenkins, 2007; Shibata et al., 2002; Taylor, Edmonds, McCarthy, & Allison, 2001; Taylor, Itier, Allison, & Edmonds, 2001; Watanabe, Mikia, & Kakigia, 2002). The majority of studies focused on an early negative ERP deflection, the N170, maximally recorded over occipitotemporal areas between 140 and 200 ms after stimulus onset and interpreted as an electrophysiological marker of the early stages of face processing representing the structural encoding (Eimer, 2000b; Rossion, Campanella, et al., 1999). These studies have shown the strong sensitivity of N170 to human faces and eyes, as reflected by larger amplitude to faces than a variety of objects (Bentin et al., 1996; Eimer, 2000b; Itier & Taylor, 2004a; Itier et al., 2006; Rossion, Campanella, et al., 1999). In these studies, the N170 for isolated eyes was greater than for other parts of the face and than for entire face (Bentin et al., 1996, 2007; Itier et al., 2006; Jemel et al., 1999; Righart et al., 2011; Shibata et al., 2002; Taylor, Itier, et al., 2001). The findings related to gaze direction showed contrasting results: in some studies, no effects of the N170 in relation to the direction of gaze were found (Klucharev & Sams, 2004; Schweinberger et al., 2007; Taylor, Itier, et al., 2001), while a larger amplitude of the N170 in the condition of the averted gaze compared to the condition of the direct gaze was found in other studies (Itier, Alain, Kovacevic, & McIntosh, 2007; Watanabe et al., 2002). Moreover, Itier, Alain, Kovacevic, et al. (2007) found a larger amplitude of late component (around 400–600 ms from stimulus presentation) in favor of the direct gaze compared to the averted. Conty, N’Diaye, Tijus, and George (2007) found that the perception of the direct gaze motion compared to the averted gaze motion elicited a greater, later and longer-lasting N170 and a greater late component (LC, P300). Finally, in an interesting study, Doi et al. (2012) reported that mothers’ N170 amplitude was larger in response to the straight gaze of their own child compared to the averted gaze. Few studies investigated how the brain processes the gaze interactions between adult faces (Carrick, Thompson, Epling, & Puce, 2007; Ulloa, Puce, Hugueville, & George, 2014) showing a specific effect of avoidant gaze between two faces in early component (M170) (Ulloa et al., 2014) and among three faces in LC (P350; P500) (Carrick et al., 2007). During the last years, the brain network involved in gaze processing has been investigated showing that averted versus direct gaze increased Amygdala

responses (Adams, Gordon, Baird, Ambady, & Kleck, 2003; Hadjikhani, Hoge, Snyder, & de Gelder, 2008; Hardee, Thompson, & Puce, 2008; Straube at al. 2010), probable neural correlate of the perception of an alert response. Others studies (Bristow, Rees, & Frith, 2007; Ethofer, Gschwind, & Vuilleumier, 2011; Pelphrey, Singerman, Allison, & McCarthy, 2003) found significantly greater activation in the parieto-frontal and in the posterior superior temporal cortex as a correlate of biological motion and socially relevant gaze processing. The involvement of parieto-frontal activation in response to gaze perception could reflect the equivalent of a mirror system in the attribution of intentions (Grosbras, Laird, & Paus, 2005). In recent studies, it has been found that different attachment styles showed different ERP components in front of emotional visual stimuli (Dan & Raz, 2012; Fraedrich, Lakatos, & Spangler, 2010; Zhang, Li, & Zhou, 2008; Zilber, Goldstein, & Mikulincer, 2007). Particularly, the avoidant attachment style showed specific differences compared to the other styles: Dan and Raz (2012) found significant early ERP differentiation between the emotional and neutral faces only within the avoidant attachment group and not within the secure or anxious group; Fraedrich et al. (2010) using the oddball paradigm found that insecure-dismissing mothers had enhanced amplitudes for the N170 component and smaller N200s and P300 in response to face stimuli compared to the secure mothers. Zhang et al. (2008) reported a lower amplitude of the N100, N200 and N400 components and a higher amplitude of the P200 component in avoidant subjects compared to secure and anxious ones in response to face stimuli. These findings suggest that avoidant attachment individuals could be characterized by an early attentive, non-conscious, discriminative brain mechanisms allowing them to later avoid negative feelings in response to emotional and relational stimuli (Dan & Raz, 2012). There are no studies yet investigating how the brain processes the gaze interaction in woman–child dyads and whether attachment dimensions are correlated with a specific brain process in response to gaze interactions. The aim of the present study was to investigate the time course of brain processes involved in the visual perception of different gaze interactions in woman–child dyads by using ERP and standardized low-resolution electromagnetic tomography (sLORETA) methodology (useful to provide a excellent compromise for analyzing both the temporal course and spatial localization of the neural processes) and the association between attachment dimensions and brain activation during the presentation of gaze interactions. The hypothesis was that the avoidant woman will produce a greater activation of

ATTACHMENT AND GAZE INTERACTIONS

primary somatosensory and limbic areas. The attachment styles dimensions avoidant-related will be associated with fronto-limbic brain intensity during the convergence of gaze.

METHOD

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Participants The study was carried out at the Clinical Neuroscience Lab of the Dynamic and Clinical Psychology Department of Sapienza University. Fifty-three young women without children took part in the study on a voluntary basis and gave informed consent for participating. All participants were students of the University “Sapienza” in Rome. All subjects were right-handed, with normal or corrected-to-normal vision and declared to be in good health and not to make habitual use of drugs or medicines. After applying electroencephalogram (EEG) data cleaning, the data of forty-four participants were included in the EEG analysis (age: M = 24.0 ± 2.5 years).

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newborn’s gaze directed in the opposite direction of the other); woman avoidance (woman’s gaze directed upward and newborn’s gaze directed toward the woman); newborn avoidance (newborn’s gaze directed upward and woman’s gaze directed towards the newborn); the control condition with neutral stimulus (houses) was inserted in order to avoid habituation of participants. The experiment began with the following instructions: “Now the images will be presented on the screen. Please, pay attention to images trying to make even less possible movements”. Each stimulus was presented for 2000 ms with an inter-stimulus interval (blank screen) varying between 1000 and 2000 ms. A total of 150 trials for each block (10 trials per condition, 3 repetitions each, 5 conditions) were presented in a random order. The interval between the two blocks lasted 60 s. The presentation order of the two blocks (faces and isolated eyes) was balanced in the sample. The experimental task duration was about 20 min.

STIMULI EXPERIMENTAL PROCEDURE The stimuli were presented using the E-Prime 2.0.8.90 Professional (2006–2010; Psychological Software Tools) on a monitor of 27 × 27 cm (75 Hz, 1024 × 768 resolution) at a viewing distance of 120 cm, in a quite dimly lit room. The experiment consisted in the presentation of images of woman–newborn couples (see Figure 1). Two blocks were presented, one with whole faces and one with isolated eyes. The five stimulus conditions were convergence (woman’s and newborn’s gaze directed toward the other); divergence (woman’s and

The visual stimuli consisted of 40 color digital images of couples “woman–newborn” (10 for each of the four condition) on a white background created using Adobe Photoshop 12.0. All the faces (cut to the neck) had neutral expression and were presented in frontal view. The woman’s and newborn’s positions were balanced on the horizontal axis of the images. The size of the faces maintained real proportions. In the isolated eyes block, two standard sized rectangles were cut out from the four conditions of faces. In the faces block, the neutral stimuli consisted of images of 10 pairs of different houses in front

Now the images will be presented on the screen. Please, pay attention to images trying to make even less possible movements

Instructions

60 s

Block 1

Figure 1. Procedure of the experimental task (total duration: about 20 min).

Block 2

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perspective, on a white background. In the isolated eyes block, the neutral stimuli consisted of two standard sized rectangles cut out from the houses’ images.

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ASSESSMENT OF ATTACHMENT Before the experiment, participants completed the Attachment Style Questionnaire (ASQ; Feeney, Noller, & Hanrahan, 1994). The Italian version of the ASQ (40 items) (Fossati et al., 2003, 2007) is a selfadministered questionnaire designed to measure five dimensions of adult attachment: Confidence (8 items), Discomfort with Closeness (10 items), Need for Approval (7 items), Preoccupation with Relationships (8 items), and Relationships as Secondary (7 items). Each item is rated on a 6-point scale. A taxometric study (Fraley & Waller, 1998) suggested the use of the scores on dimensional scales rather than in discrete categorizations. Internal consistency coefficients of the five dimensions in both clinical and nonclinical samples were good (0.64 < Cronbach’s alpha < 0.74) (Fossati et al., 2003, 2007).

EEG RECORDING AND PROCESSING OF DATA EEG was recorded continuously at 250 Hz using Net Station 4.5.1 and a 256 lead Hydrocel Geodesic Sensor Net, with impedances kept below 50 kΩ. After the acquisition, in off-line mode, the raw data were digitally filtered (30 Hz low-pass) and processed by correcting the baseline. The EEG data of each subject were segmented in epochs of 2100 ms duration, ranging from 100 ms before the presentation of the stimulus to 2000 ms from stimulus onset. Net Station artifacts detention settings were set to 200 μV for bad channels, 150 μV for the eyes blinks and 100 μV for eyes movements. The segments containing eye blinks, eye movements, or more than 10 bad channels were excluded from the analysis. The data were split in 8 time windows through visual inspection of the grand average. The time window from 80 to 132 ms was selected for the P100; the analysis on peak amplitude and latency of the P100 were conducted on the occipital montage (electrodes O1/116 and O2/150). The time window from 148 to 200 ms was selected for the N170, and the analysis on peak amplitude and latency were conducted on the temporo-occipital montage (left electrodes: 85, 95, 96, 97, 106, 107, 113,

114, 115; right electrodes: 159, 160, 161, 168, 169, 170, 171, 176). For the LCs, six intervals were selected as follows: LC1, 242–448 ms; LC2, 448–648; LC3, 648–848 ms; LC4, 848–1048; LC5, 1048–1500 ms; LC6, 1500– 2000 ms. The analysis of mean amplitude and latency for LCs were performed on temporo-occipital montage, on fronto-central montage (left electrodes: 24, 30, 34, 35, 36, 40, 41, 42, 43; right electrodes: 4, 12, 197, 206, 207, 214, 215, 223, 224).

SOURCE ANALYSES (sLORETA) To identify the locations of the neural generators of ERP components, EEG data were processed through the software GeoSource 2.0 (EGI, Eugene, OR, USA). Based on the probabilistic map, gray matter volume was parcellated into 7-mm voxels; each voxel served as a source location with three orthogonal orientation vectors. This resulted in a total of 2447 source triplets whose anatomical labels were estimated through the use of a Talairach daemon (Luciani et al., 2014). As required in the localization of the sources, it was used the dense Dipole Set (2 mm Atlas Man Dense: 2447 dipoles). The data were organized according to the criterion of cortical Gyri. In the statistical extraction, the mean intensity was extracted for each ERP component through GeoSource 2.0.

STATISTICAL ANALYSES All statistical analysis were performed using Statistica 6.1 (StatSoft, Inc. 1984–2003). ERPs evoked by the neutral stimuli (houses) were not analyzed, as they were included in the procedure only to provide a task for the subjects to maintain attention and to avoid habituation of participants (as in Taylor, Itier, et al., 2001). The ERP data for the two blocks (faces and isolated eyes) were analyzed using a 2 × 4 × 2 repeated measures analysis of variance (ANOVA) with context (faces vs. isolated eyes), gaze condition (convergence vs. divergence vs. woman avoidance vs. newborn avoidance), and hemisphere (left vs. right) as the within-subjects factors, for each window time. The dependent measures were the peak amplitude and the latency of P100, N170, and the mean amplitude and the latency for each interval of the LCs. The p-value accepted was p < .05.

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ATTACHMENT AND GAZE INTERACTIONS

For the statistical analysis on sLORETA data, paired sample t-tests between the two contexts (faces vs. isolated eyes) were performed on the mean intensity for each dipole, for all time windows considered. Only for the first block (faces), paired sample t-tests were conducted between each of four conditions of gaze (convergence vs. divergence vs. woman avoidance vs. newborn avoidance) on the mean intensity for each dipole, for all time windows considered. Bonferroni correction was applied (the p-value accepted was p ≤ .001). To test the association between attachment scores and brain intensities for each gaze conditions in the first block (faces), correlation analyses (Pearson r) were performed between the ASQ scores and the mean intensities for each brain gyrus (the p-value accepted was p ≤ .001).

RESULTS ERPs For each ERP component, an ANOVA was performed on three factors: 2 (context) × 4 (gaze) × 2 (hemispheres) (Table 1 and Figure 2). P100 showed a significant main effect of the context [F(1, 43) = 7.75, p < .0079] with a larger amplitude for faces compared to the isolated eyes and a significant effect of hemispheres [F(1, 43) = 7.06,

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p < .011] with a shorter latency on the left compared to the right hemisphere. N170 showed a significant effect of context [F(1, 43) = 7.33, p < .0097] with a larger N170 for isolated eyes than for faces and a shorter latency for faces than for the isolated eyes [F(1, 43) = 24.76, p < .00001]. An effect for hemispheres [F(1, 43) = 4.79, p < .034] with a larger N170 for the right hemisphere than for the left was also found. LC1 showed a significant effect of the context with a larger amplitude for faces than for the isolated eyes in the temporo-occipital [F(1, 43) = 8.64, p: .005] and in the fronto-central [F (1, 43) = 6.21, p: .016] in which faces showed a longer latency compared to isolated eyes [F(1, 43) = 4,77; p: .034]. A significant effect of gaze was found on latency [F(3, 129) = 3.56; p: .016] in the fronto-central area with a shorter latency in the LC1 (P350) in woman avoidance than in convergence (p = .012), divergence (p = .022), and newborn avoidance (p = .004). LC2 showed a significant effect of the context with a larger amplitude for faces than for the isolated eyes in the temporo-occipital area [F(1, 43) = 4.83; p: .033]. LC1 [F(1, 43) = 4.89; p: .032], LC3 [F(1, 43) = 10.005; p: .002], LC4 [F(1, 43) = 15.42; p: .0003], and LC5 [F(1, 43) = 9.95; p: .002] showed a significant effect of hemispheres with a larger amplitude for left than for right for the fronto-central montage.

TABLE 1 ERP data: ANOVAs: context (faces vs. isolated eyes), per gaze condition (convergence vs. divergence vs. woman avoidance vs. newborn avoidance), and per hemisphere (left vs. right) on occipital (O1–O2), temporo-occipital (TO) and fronto-central (FC) montage for P100, N170, and LCs (LC1, 242–448 ms; LC2, 448–648; LC3, 648–848 ms; LC4, 848–1048; LC5, 1048–1500 ms; LC6, 1500–2000 ms) Amplitude P100 N170

LC1

LC2 LC3 LC4 LC5 LC6

O1–O2 context, F(1, 43) = 7.75, p = .008 Faces > eyes TO—CONTEXT, F(1, 43) = 7.33, p = .009 Faces < eyes TO—HEMIS, F(1, 43) = 4.79, p = .034, R > L FC—CONTEXT, F(1, 43) = 6.21, p = .016 Faces > eyes FC—HEMISF, F(1, 43) = 4.89, p = .032, R < L TO—CONTEXT, F(1, 43) = 8.64, p = .005 Faces > eyes

TO—CONTEXT, F(1, 43) = 4.83, p = .033 Faces > eyes FC—HEMISF, F(1, 43) = 10.005, p = .002, R < L FC—HEMISF, F(1, 43) = 15.42, p = .0003, R < L FC—HEMISF, F(1, 43) = 9.95, p = .002, R < L /

Latency O1–O2 HEMIS, F(1, 43) = 7.06, p = .011, R > L TO—CONTEXT, F(1, 43) = 24.76, p = .0001 Faces < eyes FC—CONTEXT, F(1, 43) = 4.77, p = .034 Faces > eyes FC—GAZE, F(3,129) = 3.56, p = .016 Woman avoidance < convergence (p = .012) Woman avoidance < divergence (p = .02) Woman avoidance < newborn avoidance (p = .004) FC—HEMISF, F(1, 43) = 10.71, p = .002, R < L TO—HEMISF, F(1, 43) = 5.32, p = .025, R < L / / / / /

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Figure 2. Sensor-level grand averages of temporo-occipital montages for faces versus eyes and of fronto-central montages for the four conditions of gaze. Note the higher amplitude of faces compared to eyes in temporo-occipital montages in the P100 components and the different amplitudes of woman avoidance compared to convergence, divergence, and newborn avoidance in fronto-central montages in the LC1 (350 ms)components.

LC1 showed a significant effect of hemispheres with a longer latency for left than for right in the fronto-central [F(1, 43) = 10.71; p: .002] and in the temporo-occipital [F(1, 43) = 5.32; p: .025]. sLORETA Paired sample t-tests (see Table 2) showed a significantly greater intensity for faces compared to the isolated eyes: in the right extranuclear (at P100, p = .000002; N170, p = .002; LC1, p < .00001), in the left anterior cingulate (at P100, p = .0002; LC2, p = .006), and in the right cuneus (at P100, p = .000001; N170, p < .00001). For the faces block, paired sample t-tests conducted between each of four conditions of gaze showed a significantly greater intensity for woman avoidance vs. convergence in the left angular gyrus (at P100, p < .00001; N170, p < .00001; LC1, p = .000001; LC2, p < .00001; LC3, p < .00001; LC4, p < .00001), in the right angular gyrus (P100, p = .000001; LC2, p = .00007; LC3, p = .000005; LC4, p = .003), in the left extranuclear (P100, p < .0001; N170, p < .00001; LC1, p = .00005; LC2, p < .00001; LC3, p < .00001; LC4, p < .0001), in the left and right anterior cingulate (at LC2, p = .001, p = .005; LC3, p < .00001, p = .00002; LC4, p < .00001, p = .004, respectively), and in the left and right cuneus (at LC4, p = .0005, p = .005, respectively).

A greater intensity was also seen for woman avoidance vs. divergence in the left angular gyrus (at P100, p < .00001; N170, p < .00001; LC1, p = .004; LC2, p = .000007; LC3, p = .00003; LC4, p < .00001), in the right angular gyrus (at P100, p = .00003; N170, p = .000001), in the left extranuclear (at P100, p = .00001; N170, p < .00001; LC3, p = .0008; LC4, p < .00001), in the left cuneus (at LC4, p = .001), in the right cuneus (at LC3, p = .0002; LC4, p < .00001), in the left inferior frontal gyrus (at LC4, p = .002), and in the right lingual gyrus (at LC4, p = .00015). A greater intensity for woman avoidance vs. newborn avoidance in the left angular gyrus (at P100, p < .00001; N170, p < .00001; LC1, p = .0006), in the right angular gyrus (at P100, p < .00001), in the right extranuclear (at P100, p < .00001; LC1, p = .001), in the right anterior cingulate (at P100, p = .008), and in the left fusiform gyrus (at P100, p = .002). Only the right extranuclear showed a greater intensity for the divergence vs. newborn avoidance (at P100, p = .00001). The newborn avoidance showed a greater intensity compared to the convergence in the left angular gyrus (at LC3, p < .00001; LC4, p < .00001) and in the right angular gyrus (at LC3, p = .006). The newborn avoidance showed a greater intensity compared to the divergence only in the left angular gyrus (at LC4, p = .000003).

Left anterior cingulate

LC2

LC4

LC3

Right extranuclear

LC1

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Attachment style dimensions are associated with brain activity in response to gaze interaction.

Aim of the present study was to investigate the time course of brain processes involved in the visual perception of different gaze interactions in wom...
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