PHB-10458; No of Pages 9 Physiology & Behavior xxx (2014) xxx–xxx

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Michela Balconi a,b,⁎, Silvia Pagani a a

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Keywords: BIS-BAS Social ranking Alpha band Cognitive performance Peer-group Self-perception

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1. Introduction

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The perception and interpretation of social hierarchies seem to be a key part of our social apparatus and have an evident impact upon our physical and psychological well-being. However, there had been little

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research aimed at identifying those brain areas and psychological factors involved in this high-order process, that is, the judgment of social hierarchies [35,37]. It is no surprise that in humans as well as other primates differential positions within social hierarchies are predictive of the individual's physical condition [1], mental well-being [2], neurocognitive functioning [33] and, in extreme cases, even survival [36]. In addition, the ability to infer accurately one's own status and the status of others in a social hierarchy is crucial to successful social interaction. Indeed, social hierarchies spontaneously and rapidly emerged in newly-formed groups of individuals, possibly because of the mutual agreement on inferences about others' competence and power [19,33].

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The perception and interpretation of social hierarchies are a key part of our social life. In the present research we considered the activation of cortical areas, mainly the prefrontal cortex, related to social ranking perception in conjunction with some personality components (BAS – Behavioral Activation System – and BIS – Behavioral Inhibition System). In two experiments we manipulated the perceived superior/inferior status during a competitive cognitive task. Indeed, we created an explicit and strongly reinforced social hierarchy based on incidental rating in an attentional task. Specifically, a peer group comparison was undertaken and improved (Experiment 1) or decreased (Experiment 2) performance was artificially manipulated by the experimenter. For each experiment two groups were compared, based on a BAS and BIS dichotomy. Alpha band modulation in prefrontal cortex, behavioral measures (performance: error rate, ER; response times, RTs), and self-perceived ranking were considered. Repeated measures ANOVAs and regression analyses showed in Experiment 1 a significant improved cognitive performance (decreased ER and RTs) and higher self-perceived ranking in high-BAS participants. Moreover, their prefrontal activity was increased within the left side (alpha band decreasing). Conversely, in Experiment 2 a significant decreased cognitive performance (increased ER and RTs) and lower self-perceived ranking was observed in higher-BIS participants. Their prefrontal right activity was increased in comparison with higher BAS. The regression analyses confirmed the significant predictive role of alpha band modulation with respect of subjects' performance and self-perception of social ranking, differently for BAS/BIS components. The present results suggest that social status perception is directly modulated by cortical activity and personality correlates. © 2014 Published by Elsevier Inc.

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Article history: Received 31 January 2014 Received in revised form 11 April 2014 Accepted 28 May 2014 Available online xxxx

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BIS-BAS constructs modulate social ranking perception. Higher-BIS subjects were more responsive to decreased social ranking. Higher-BAS subjects were more responsive to increased social ranking. Prefrontal brain activity affects self-perception of ranking. Alpha band modulation and personality trait influenced the cognitive performance.

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Laboratory of Cognitive Psychology, Department of Psychology, Catholic University of the Sacred Heart, Milan, Italy Research Unit in Affective and Social Neuroscience

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Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison

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⁎ Corresponding author at: Department of Psychology, Catholic University of the Sacred Heart, Milan Largo Gemelli, 1, 20123, Milan, Italy. Tel.: +39 2 72342586; fax: + 39 2 72342280. E-mail address: [email protected] (M. Balconi).

http://dx.doi.org/10.1016/j.physbeh.2014.05.043 0031-9384/© 2014 Published by Elsevier Inc.

Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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The BAS system should be responsible for both approach and active behaviors, and emotions associated with these behaviors generally induce the subject to approach to event/object that have generated the emotional response. The BAS is conceptualized as a motivational system that is sensitive to signals of reward, non-punishment, and that is important for engaging behavior toward a reward or away from a threat. Moreover, BAS has been associated with feelings of optimism, happiness, aggression and dominance [6,7,21,24]. Empirical evidence suggests that people with highly sensitive BAS may respond in great measure to positive, approach-related emotions, such as the expression of happiness and positive affect, that allow the subject to have a favorable and dominant behavior toward the environment [3–5,15,40]. Conversely, highly sensitive BIS people inhibit behavior in response to stimuli that are novel, innately feared, and conditioned to be aversive. The aversive motivational system is responsive to non-reward, avoiding to experience of negative or painful outcomes. Thus, the BIS is conceptualized as an attentional system that is sensitive to cues of punishment and non-reward, and that functions to interrupt ongoing behavior in order to facilitate the processing of these cues in preparation for a response. In the BIS framework “inhibition” refers to the abrogation of behavior in reaction to an expected or unexpected stimulus [20,41]. Gray also held that BIS functioning is responsible for the experience of negative feelings such as fear and anxiety in response to these cues [23,22]. Thus both our personality and our personal perception of social position and hierarchy may interact to impact our social success and sense of well-being. That is, self-perception of our position within the social ranking and our personality component related to reward mechanisms may influence the effective social relationship and the social ability to stay with other people. Therefore, an integrative approach, combining both measures of self-perception and BIS/BAS mechanism, is needed in order to achieve a comprehensive understanding of the neurophysiological substrates implicated in hierarchy-related behaviors, mediated by the personality component of reward responsiveness. From the neuroanatomical point of view, the cortical correlates of the BIS/BAS system are the PFC, and left PFC was shown to be implicated in approach-related motivations and emotions, whereas the right PFC was found to be involved in withdrawal-related motivations and emotions [8,9]. Empirical data suggest that left and right frontal activity may reflect the strength of BAS and BIS activity respectively [6]. Due to the controlateral inhibition between the hemispheres, the lateralized approach and withdrawal or punishment-reward system are mutually inhibitory. The role of the reward system (BAS), on the one hand, and that of the frontal brain area, on the other, was supposed to be able to elucidate the dominance mechanisms. Thus, we may suppose that, based on the lateralized reward/ punishment model, there are different contributions of the left and right hemispheres on self-perception of social ranking. It should be plausible that the hemispheric “competition” between the left and right sides would characterize social hierarchy behavior, showing a higher BAS reward attitude in “dominance conditions” with an imbalance in favor of the left hemisphere. Reward system effect (BIS/BAS), social hierarchy perception as a function of subjects' personal performance in comparison with others' performance, and cortical responsiveness, were not previously evaluated together in detail. The effect of BIS/BAS on social ranking perception and the impact of this personality component on the frontal brain network were tested in the present research. The BIS/BAS component was considered a key factor in explaining the relationship between subjects' cognitive performance and self-perception of social status. The BIS/BAS construct was also considered an explicative factor, one able to explain the frontal brain contribution in social status representation. That is, the brain responsiveness was examined in relationship with the BIS/BAS dichotomy and the self-perceived status hierarchy status based on performance rating. To study the effect of ranking related to the subject's performance we modified the superior/inferior status during a competitive task.

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The quick emergence in social interactions is mirrored by its early appearance during ontogeny: two-year-old children are able to assemble stable, linearly transitive dominance hierarchies [11]. The pervasive impact of social status and dominance brought many researchers to examine the neurophysiological correlates of how social ranks are perceived, formed and maintained. However, only in the past few years have biopsychologists begun to explore how the brain processes information about social hierarchies (for a review, see Chiao [13]). Recent social neuroscience studies show that distinct neural systems are involved in the recognition and experience of social hierarchy, and that activity within these brain regions is modulated by individual and cultural factors. Levitan et al. [28] theorizes that a neural circuit linking limbic, prefrontal cortex, and striatal structures reflect the emotional, cognitive, and behavioral components of rank-related social interactions. Recent investigations examining the structure and function of brain areas associated with social rank offer preliminary support for this neural mechanism of a human social rank system. Dorsal and ventral portions of lateral prefrontal cortex – brain regions typically associated with regulating socioemotional responses and behavioral inhibition, respectively – are recruited during social status inference [14], particularly when people infer dominance in others from bodily postures [31,32] and symbols [42]. The engagement of DLPFC and VLPFC regions during the observation of dominant individuals probably reflects recruitment of brain regions that can exert top-down control over automatic processes, such as emotional responses to social hierarchy, to orchestrate a socially appropriate status response [31]. However, in our opinion, it is crucial to consider the implication of cortical areas, mainly the prefrontal cortex, which was shown to be activated in response to social ranking perception in conjunction with some specific subjective (self-perception of status) and personality components. Indeed, on the one hand, the perception and interpretation of social hierarchies may be self-referential, relating to a person's own perceived position within them. In human beings, social hierarchies can be established along various dimensions: we can be ranked according to ability or skill, as well as economic, physical, and professional standing. Previous research suggested an important role for hierarchical rank in achieving accurate self-knowledge and self-improvement, particularly in the usage of upward social comparisons performance-related. This is the specific analysis of the social status in the context of performancebased feedback [42]. This direct comparison on a specific task may or may not improve our rank perception, taking into account the existing hierarchy. Moreover, it was also shown that social status perception affects performance on tasks that involve comparing our own performance with that of others [42]. In a previous experiment, Zink et al. [42] used fMRI to measure brain activation in participants presented with an interactive performance in which simulated players were manipulated to be either superior or inferior in task-related skills. The simulated players' statuses were held constant in a contrived “stable hierarchy” condition and allowed to vary periodically during a contrived “unstable hierarchy” condition. Results indicated that in a stable hierarchy, viewing a superior, relative to an inferior player activates bilateral occipital/parietal cortex, striatum, parahippocampal cortex, and dorsolateral prefrontal cortex. No unique activation associated with viewing an inferior player was identified. On the other hand, the way that individuals judge such social ranking positions may partially depend on intrinsic personality factors such as the degree to which their own behavior is balanced between “approaching” in response to rewards and non-punishments (the Behavioral Activation System, BAS, [23]) and “withdrawing” from nonreward and punishments (the Behavioral Inhibition System, BIS) [17]. In one previous study it was found that subjects with a higher BAS were more likely to relate to the dominant character in a presented dyad, which was found to induce a positive effect, while those with a higher BIS were more inclined to relate to the submissive character, inducing a negative affect [16].

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Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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2. Method

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2.1. Subjects

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Seventy-one undergraduate students took part in the experiment: thirty-three for Experiment 1 (eighteen men; age range of subjects: 19–27, M = 25.34, SD = 1.01) and thirty-eight for Experiment 2 (twenty men; age range of subjects: 19–26, M = 25.02, SD = 1.05). The participants were all right-handed and presented normal or corrected-to-normal visual acuity, and they gave informed written consent to participate in the study. Exclusion criteria were history of psychopathology (Beck Depression Inventory, BDI-II) [10] for the subjects and immediate family. State-Trait-Anxiety-Inventory (STAI) [39] was submitted after the experimental session. No neurological or psychiatric pathologies were observed. Two expert clinicians applied a semistructured interview and evaluated the general psychopathological profiles of the subjects and their direct family's members, in a preliminary phase of the research. No payment was provided for subjects' performance. The research was approved by the local ethics committee of the Department of Psychology, Catholic University of Milan. Exclusion criteria were a history of psychopathology in the subjects or their immediate family.

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Subjects were seated comfortably in a moderately lighted room with a monitor screen positioned approximately 60 cm in front of their eyes. They performed a simple task for sustained selective attention: they were told that some cognitive attentional measures were used to evaluate the subjective skills and that these measures were usually applied as screening to test future professional career success. Specifically, they were told that the scoring was based on the response inaccuracy (number of error: ER, error rate) and response times (RTs). Subjects were required to select a target stimulus between non-targets, based on four different options of shape/color: the stimuli might interchangeably be a triangle or a circle, colored red or green. They were required to distinguish between target/non-target by focusing attention on each stimulus. The target was displayed on the video (indicated as the target for selection) and the successive stimuli were presented one after another. The target stimulus features changed every 25 trials. The subjects were instructed to make a two-alternative forced-choice response by pressing a left/right button. The bottom was counterbalanced across subjects. Each stimulus was presented for 2 sec, preceded by a fixation point (a centered cross), and subjects had 1 sec to produce a response. After this time the subjects could not respond. Stimuli were presented in a randomized order in the center of the computer monitor, with a horizontal angle of 9° and a vertical angle of 11.8° (E-prime 2.0 software, temporal resolution 10 ms). Accuracy and speed were stressed. To stress the RTs, subjects were told that the performance evaluation was based on the RTs in addition to the accuracy of the response. A familiarization phase allowed them to comprehend the significance of the task and to learn the detection procedure. Subjects were also told that their performance was constantly compared with that of other young subjects, who had similar profiles (young university students), to define their ranking position. Every three trials, the subject would be informed of his/her performance based on the comparison with the peer group's performance. The performance feedback was signaled by two up-arrows (performance better than 75% compared with peer group); one line (mean performance) and two down-arrows (performance worse than 75% compared with peer group). The task was composed of 100 trials. After each block of 25 trials (each block corresponded to one interval, for a total of four intervals), subjects were required to evaluate their performance in comparison with the peer group on a seven-point Likert scale (from one = most decreased performance, to seven = most improved performance) (Fig. 1). Covertly, outcomes were fixed, and in Experiment 1 the subjects were told they had a performance better than the comparison group. Across the task, after the initial mean performance, subjects were constantly reinforced about their good performance by being told that they ranked better than the mean profile (up-arrows, only 30% were better than them). Only sometimes were they told their performance was under the mean (three times in total) to make the task more credible. In Experiment 2 subjects were told their performance was worse than the comparison group. Indeed, after an initial mean performance, they were informed of their bad performance (only 30% were worse than them). The feedback system continually reinforced the hierarchy by being displayed throughout the session. Implicit symbolic cues related to social superiority (up and down arrow) were used. The nature of the task (similar comparative group, professional application of the test and online monitoring) ensured that the hierarchical status of the other competitor had real perceived impact. Participants were strongly engaged in the hierarchical context (92% told to be strongly engaged), as was evident by post-session questionnaire data. The subjects were also required to self-report their degree of trust of the exact feedback of the performance, which showed high trust (96%), a relevance of the task for social status (94%), the perceived ranking position during the task (93%), with high- (Experiment 1, 92%) vs. low-ranking (Experiment 2, 94%).

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The subject's scoring on a cognitive task, which dynamically modulated the subject's perceived status, was artificially manipulated. Thus, in two experiments, we created an explicit and strongly reinforced social hierarchy based on incidental skill in the context of an interactive task. In contrast with previous studies [42], we included a more ecologic task, where subjects were required to compare their performance constantly with that of other people. Specifically, a peer group comparison was performed because the dynamic changes of the subjects' performance (an improved – Experiment 1 – or decreased – Experiment 2 – performance artificially manipulated by the experimenter) were compared with the performance of the peer group. This comparison tested the effect of the subject's own status modification related to the group's status. The real performance was also tested (better or worse attentional performance) in response to this fictitious increasing or decreasing scoring. Based on our hypotheses, we supposed that higher BAS participants may respond in greater measure to increased social status (Experiment 1) than decreased social status (Experiment 2), based on their sensitivity to rewarding and high dominant conditions. On the contrary, higher BIS participants should respond in greater measure to decreased social status as a less rewarding situation and potentially “punishing” condition. Therefore decreased alpha activity (i.e. increased brain responsiveness) should be found respectively for higher BAS in the frontal left brain area in perceived increased social ranking, whereas decreased alpha activity (i.e. increased brain responsiveness) should be found for higher BIS in the frontal right area in perceived decreased social ranking. Concerning real cognitive performance, consistent better performance should be found for higher BAS (and partially for BIS) in the case of perceived higher ranking, as an effect of a more reinforcing condition. This “improving performance effect” should be more significant in a higher BAS as a concomitant effect of perceived dominance and reward, which higher BAS estimates in greater measure. That is we may find consistent and higher differences across experiments for higher BAS and BIS owing to high sensitivity to reward or punishment respectively. Finally, a significant relationship should be found between these multiple measures, since we expected an increased frontal left brain activity mainly in higher BAS, and that this activity should be related firstly with a better performance and secondly with the self-perception of an increased social ranking in the case of Experiment 1. On the contrary, increased frontal right activity, mainly in higher BIS, should be related to worse performance and the self-perception of decreased social ranking in case of Experiment 2.

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Fig. 1. Experimental task and procedure.

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BIS and BAS scores were calculated for each subject by using the Italian version of Carver and White Questionnaire (1994) (Leone, Pierro, & Mannetti, 2002). It included 24 items (20 score-items and 4 fillers, each measured on four-point Likert scale), and two total scores for BIS (range = 7–28; items 7) and BAS (range = 13–52; items 13). BAS also includes three subscales (Reward, 5 items, Drive, 4 items, and Fun Seeking, 4 items). The questionnaire was submitted to the subject after completing the experimental phase (three days later). Based on these measures, two total scores (BIS and BAS total) and three BAS subscale scores were calculated. The mean values and standard deviations for each scale were respectively for Experiment 1: BIS: 19.11 (2.70); BAS: 38.55 (2.89); Reward: 15.33 (1.90); Drive: 13.28 (2.23); Fun Seeking: 11.80 (3.10); for Experiment 2: BIS: 19.34 (2.34); BAS: 38.10 (2.30); Reward: 15.78 (1.89); Drive: 13.21 (2.67); Fun Seeking: 11.55 (2.98). Finally, Cronbach's alpha was calculated for BIS (0.92) and BAS (0.90) and separately for each BAS subscale (Reward 0.89; Drive 0.88, and Fun Seeking 0.87). Based on these sub-scale ratings we considered two sub-groups of subjects: high-BAS and high-BIS subjects. The first group includes subjects with high BAS (more than 40, mean + 1 SD); the second group includes subjects with high BIS (more than 21, mean + 1 SD). With respect of the two Experiments, we included 30 subjects for the final analysis (16 high BAS and 14 high BIS) for Experiment 1, and 33 subjects for Experiment 2 (17 high BAS and 16 high BIS). The other subjects (respectively three and five subjects for the two Experiments) were not included since they showed a mixed profile taking into account BIS/BAS scoring.

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EEG recordings were performed with a 64-channel DC amplifier (SYNAMPS system) and acquisition software (NEUROSCAN 4.2) during task execution. An ElectroCap with Ag/AgCl electrodes was used to record EEGs from active scalp sites referred to the earlobes (10/20 system of electrode placement, [25]). Data were acquired using a sampling rate of 500 Hz, with a frequency band of 0.01–40 Hz. An off-line common average reference was successively computed to limit the problems associated with the signal-to-noise ratio [29]. Additionally, two EOG electrodes were sited on the outer canthi to detect eye movements.

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2.5. Data analysis

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Four sets of analyses were performed with respect to behavioral (error rate, ER; response times, RTs; ranking self-perception) and alpha band measures for each experiment. Repeated measure ANOVAs were applied to these dependent measures with independent withinsubjects factors: group (BAS vs. BIS), and time (four intervals) applied to ER, RTs and self-perception variables; group, hemisphere side (left vs. right), and time applied to alpha band variable. Indeed, a total score was calculated every 25 trials (four total scores for the intervals) to explore the modulation of subjects performance, ranking perception and alpha band changes during the task. The RTs were recorded from the stimulus onset, and ER was calculated as the total number of incorrect detections out of the total trial for each category. Higher values represented increased incorrect responses. Alpha band modulation was calculated every 25 trials. For all of the ANOVA tests, the degrees of freedom were corrected using Greenhouse–Geisser epsilon where appropriate. Post-hoc comparisons (contrast analyses) were applied to the data. A successive regression analysis was applied to EEG and behavioral (performance and self-perception) measures, distinctly for BAS and

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The impedance of the recording electrodes was monitored for each subject prior to data collection and was always below 5 kΩ. After performing EOG correction and visual inspection, only artifact-free trials were considered (rejected epochs, 2%). The signal was visually scored, and portion of the data that contained artifacts was removed to increase specificity. Blinks were also visually monitored. Ocular artifacts (eye movements and blinks) were corrected using an eye-movement correction algorithm that employs a regression analysis in combination with artifact averaging [35,38]. We measured left and right frontal (F3, F4) alpha power activity. The digital EEG data were bandpass filtered in the frequency band 8–12 Hz (band-pass filtering 96 dB/octave roll off, warm-up filter left and right to 100 ms). To obtain a signal proportion to the power of the EEG frequency band, the filtered signal samples were squared [34]. An average absolute power value for each experimental condition (see the following data analysis) was calculated. An average of the pre-experimental absolute power (− 200 ms) was used to determine the individual power during no stimulation. For the statistical analysis the two frontal electrode positions (F3, F4) were considered.

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Table 1 Mean error rates (ERs), response times (RTs, msec.) for each interval.

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3.1.3.1. EEG (alpha band) measure. ANOVA indicated significant effect for group (F[1,29] = 8.44, p ≤ .001, η2 = .38), group × side (F[1,29] = 9.80, p ≤ .001, η2 = .42), and group × side × time (F[3,29] = 9.33, p ≤ .001, η2 = .41) (Table 2). Higher BAS showed a significant alpha decreasing (increased cortical activity) compared with higher BIS. Secondly, this decreased alpha band was higher within the left more than the right hemisphere (F[1,29] = 7.16, p ≤ .001, η2 = .36) only for higher BAS. Finally, the alpha band decreasing for BAS was more accentuated within the third (F[1,29] = 7.98, p ≤ .001, η2 = .37) and four (F[1,29] = 9.55, p ≤ .001, η2 = .40; F[1,29] = 8.04, p ≤ .001, η2 = .38)

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Fig. 2. Self-perceived ranking as a function of BAS/BIS and different time intervals.

time in comparison with respectively the first the second time (Fig. 3). 448 No other effect was significant. 449

3.1.2. RTs Differences were found for group (F[1,29] = 9.18, p ≤ .001, η2 = .41) and group × time (F[3,29] = 7.78, p ≤ .001, η2 = .36). Decreased RTs were found for higher BAS more than higher BIS. Moreover, as revealed by contrast analysis, second (F[1,29] = 9.03, p ≤ .001, η2 = .41), third (F[1,29] = 9.74, p ≤ .001, η2 = .42) and fourth (F[1,29] = 8.60, p ≤ .001, η2 = .39) time showed reduced RTs in comparison with the first time only for higher BAS. 3.1.3. Ranking self-perception ANOVA indicated significant effect for group (F[1,29] = 8.70, p ≤ .001, η2 = .38) and group × time (F[3,29] = 9.09, p ≤ .001, η2 = .40). Higher BAS showed an increased self-perception of high ranking in comparison with higher BIS. Secondly, this increased perception was more accentuated in the third (F[1,29] = 9.06, p ≤ .001, η2 = .38; F[1,29] = 7.10, p ≤ .001, η2 = .36) and four (F[1,29] = 9.13, p ≤ .001, η2 = .39; F[1,29] = 7.15, p ≤ .001, η2 = .35) time in comparison with respectively the first the second time for higher BAS (Fig. 2). No significant effects were found between the four intervals for higher BIS.

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3.1.4. Regression analysis between alpha band and ERs, RTs and ranking perception measures Two distinct multiple regressions for BAS and BIS participants were applied to the data, considering left and right alpha band modulation

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Table 2 Multiple regression for BAS (a) and BIS (b) participants.

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3.1.1. ER ANOVA indicated significant effect for group (F[1,29] = 7.78, p ≤ .001, η2 = .36) and group x time (F[3,29] = 9.61, p ≤ .001, η2 = .41) (Table 1). Higher BAS showed a decreased ER in comparison with higher BIS. Secondly, ER decreased in the second (F[1,29] = 9.06, p ≤ .001, η2 = .39), third (F[1,29] = 7.18, p ≤ .001, η2 = .36) and four (F[1,29] = 8.51, p ≤ .001, η2 = .38) time in comparison with the first time for higher BAS. No significant effects between the four intervals were found for higher BIS.

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BIS group. Finally, a successive direct comparison was made between Experiment 1 and Experiment 2, applying a repeated measure ANOVA to behavioral and alpha band dependent variables with three or four independent factors: experiment (2) × group (2) × side (2) × time (4).

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0.20 0.04 0.30 0.17 1.22

RTs R R2 β std error t

0.22 0.05 0.32 0.22 1.28

0.23 0.05 0.28 0.30 1.32

Rating R R2 β std error t

0.18 0.03 0.38 0.21 0.98

0.13 0.01 0.31 0.28 0.55

⁎ p = .05. ⁎⁎ p = .01.

Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

t2:3 Q2 t2:4 t2:5 t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23 t2:24 t2:25 t2:26 t2:27 t2:28 t2:29 t2:30 t2:31 t2:32 t2:33 t2:34 t2:35 t2:36 t2:37 t2:38 t2:39 t2:40 t2:41 t2:42 t2:43 t2:44 t2:45 t2:46 t2:47 t2:48

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second third time intervals

fourth

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Fig. 4. Self-perceived ranking as a function of BAS/BIS and different time intervals.

3.2. Experiment 2

462 463

3.2.1. ER ANOVA indicated significant effect for group (F[1,32] = 8.11, p ≤ .001, η2 = .39) and group × time (F[3,32] = 8.80, p ≤ .001, η2 = .40) (Table 3). A significant increased ER was found for BIS more than BAS. Moreover, as revealed by post-hoc comparisons, ER showed an increasing in the second (F[1,32] = 9.22, p ≤ .001, η2 = .42), third (F[1,32] = 7.12, p ≤ .001, η2 = .36) and four (F[1,32] = 9.54, p ≤ .001, η2 = .43) time in comparison with the first time for BIS. On the contrary BAS showed more stable ER values without significant differences between the four intervals.

469 470 471 472 473 474 475 476

3.2.2. RTs Significant differences were found for group (F[3,32] = 9.96, p ≤ .001, η2 = .45). Consistent increased RTs were found for BIS in comparison with BAS. No other effect was statistically significant.

t5:1 t5:2

Table 3 Mean error rates (ERs), response times (RTs, msec.) for each interval.

3.2.2.3. Regression analysis between alpha band and ERs, RTs and ranking perception measures. Two distinct multiple regressions for BAS and BIS participants were applied to the data. As shown in Table 4a, b for BIS, right alpha account mainly for ERs, RTs and self-perception, that is the decreased right alpha explains the ER and RT increasing and ranking self-perception decreasing. On the contrary left alpha did not account for the predicted variable modulation. For BAS, no significant effects were found, since alpha band modification was not significant in explaining the predicted variables.

496

E

N

8.00 7.00

U

t5:3

ERs

t5:4

M

t5:5 t5:6 t5:7 t5:8 t5:9 t5:10 t5:11 t5:12 t5:13 t5:14 t5:15

485

C

479

3.2.2.1. Ranking self-perception. ANOVA indicated significant effect for group (F[1,32] = 8.15, p ≤ .001, η2 = .38) and group × time (F[3,32] = 7.80, p ≤ .001, η2 = .36). Higher BIS showed a decreased self-perception of high ranking in comparison with higher BAS.

477 478

3.2.2.2. EEG (alpha band) measure. ANOVA indicated significant effect for group (F[1,32] = 8.40, p ≤ .001, η2 = .38), group × side (F[1,32] = 9.15, p ≤ .001, η2 = .41), and group × side × time (F[3,32] = 8.56, p ≤ .001, η2 = .39). Indeed, higher BIS showed alpha decreasing (increased cortical activity) compared with higher BAS. Secondly, this decreased alpha band was higher within the right more than the left hemisphere (F[1,32] = 7.75, p ≤ .001, η2 = .36) only for higher BIS. Finally, the alpha band decreasing for BIS was more accentuated within the second (F[1,32] = 9.02, p ≤ .001, η2 = .39; third (F[1,32] = 8.11, p ≤ .001, η2 = .38) and four F[1,32] = 8.59, p ≤ .001, η2 = .38) time in comparison with the first (Fig. 5). No other effect was significant.

T

C

E

467 468

R

465 466

R

464

O

457 458

480

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Secondly, this decreased perception was more accentuated in the second (F[1,32] = 9.44, p ≤ .001, η2 = .39), third (F[1,32] = 8.88, p ≤ .001, η2 = .38) and four (F[1,32] = 9.10, p ≤ .001, η2 = .39) time in comparison with the first time (Fig. 4). No other significant effect was found.

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as predictor variables and ERs, RTs and self-perception as predicted variables. As shown in Table 2a, b for BAS, left alpha account mainly for ERs, RTs and self-perception, that is the decreased left alpha explains both the ER and RT decreasing and self-perception increasing. On the contrary right alpha did not account for the predicted variable modulation. For BIS, no significant effects were found, since alpha band modification was not significant in explaining the predicted variables.

BAS First Second Third Fourth BIS First Second Third Fourth

0.08 0.07 0.07 0.06

RTs (SD) 0.02 0.01 0.02 0.02

M 511 508 512 510

(SD) 12 17 15 17

alpha band power

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Fig. 3. Mean power of alpha in left and right side as a function of BAS/BIS and different time intervals.

*

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1.00 0.00 le

0.09 0.12 0.12 0.13

0.01 0.02 0.02 0.02

543 555 561 550

15 16 18 20

right BAS

le

right BIS

Fig. 5. Mean power of alpha in left and right side as a function of BAS/BIS and different time intervals.

Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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Predictors

Left alpha⁎

Right alpha

a ER R R2 β std error t

0.22 0.06 0.42 0.16 0.68

0.13 0.01 0.30 0.21 0.80

RTs R R2 β std error t

0.20 0.04 0.32 0.17 0.60

0.14 0.01 0.30 0.28 0.51

Rating R R2 β std error t

0.11 0.00 0.34 0.12 0.50

0.16 0.03 0.30 0.20 0.60

t4:47 t4:48

⁎ p = .05. ⁎⁎ p = .01.

505

3.3. Comparison between Experiment 1 and 2

506

3.3.1. ER ANOVA indicated significant effect for group × experiment (F[1, 61] = 8.13, p ≤ .001, η2 = .39) and group × experiment × time (F[3, 61] = 8.61, p ≤ .001, η2 = .40). As shown by post-hoc comparisons applied to two-way interaction, a significant decreased ER was found in Experiment 1 compared with Experiment 2 for higher BAS (F[1, 61] = 8.54, p ≤ .001, η2 = .39), whereas an increased ER was observed in Experiment 2 compared with Experiment 1 for higher BIS (F[1, 61] = 8.13, p ≤ .001, η2 = .37). Moreover, as revealed by posthoc comparisons applied to three-way interaction, in the Experiment 1 ER decreased in the second (F[1, 61] = 8.45, p ≤ .001, η2 = .39), third (F[1, 61] = 6.57, p ≤ .001, η2 = .35) and four (F[1, 61] = 10.08, p ≤ .001, η2 = .47) time in comparison with the Experiment 2 for higher BAS. On the contrary, in the Experiment 2 ER decreased in the second (F[1, 61] = 8.15, p ≤ .001, η2 = .39), third (F[1, 61] = 6.95, p ≤ .001, η2 = .36) and four (F[1, 61] = 10.99, p ≤ .001, η2 = .48) time in comparison with the Experiment 2 for higher BIS.

511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526

0.14 0.02 0.31 0.16 0.92

0.55 0.28 0.35 0.20 4.77⁎⁎

F

O

R O

Rating R R2 β std error t

E R R

3.3.2. RTs Significant effects were found for group × experiment (F[1, 61] = 8.10, p ≤ .001, η2 = .40). Based on post-hoc comparisons, significant decreased RTs were found in Experiment 1 compared with Experiment

533 534 535 536 537 538 539 540 541 542 543

4. Discussion

557

The present research explored the contribution of personality factor (BAS and BIS construct) in social ranking perception and subjective performance during a cognitive task. As supposed in our hypotheses, the main results pointed out that BAS/BIS dichotomy may explain the subjects' response to a perceived positive and improved social ranking (artificially increased, Experiment 1) and to a negative and decreased social ranking (artificially decreased, Experiment 2). Secondly, cognitive performance was affected by the external feedback in terms of ranking manipulation. Indeed an induction of perceived worse performance (worse than the peer group) determined a real worse-rating for both ER and RTs, mainly in higher BIS subjects, whereas a perceived improved performance (better than peer group) determined a real better-rating, mainly in higher BAS subjects. Thirdly, the role of the frontal brain correlates in modulating hierarchy perception was analyzed, taking into account the alpha band changes within the left and right frontal side. Indeed the modification of right/left hemisphere activity was considered to explain the subject's perception and execution of his/her performance in comparison with the peer group's performance. These main points are elucidated. First, the present research pointed out that hierarchical status perception may partially depend on intrinsic personality factors such as the degree to which subjects' behavior is balanced between “approaching” in response to rewards and non-punishments (BAS) and “withdrawing” from non-rewards and punishments (BIS). Indeed, BAS subjects showed a significant increased self-perception of high ranking status in the case of the reinforcing situation, where participants were told they have an improved performance in comparison with a peer group (Experiment 1). That is, the induced higher ranking condition was perceived as really positive and of an “increased status”. In contrast, higher BIS did not appear to be able to consider the external feedback which pointed out the higher ranking position in comparison

558

P

0.44 0.20 0.20 0.36 4.09⁎⁎

531 532

544

D

0.20 0.05 0.35 0.28 1.20

530

3.3.4. EEG (alpha band) measure ANOVA indicated significant effect for group × side (F[1, 61] = 9.10, p ≤ .001, η2 = .41), and experiment × group × side (F[1, 61] = 8.56, p ≤ .001, η2 = .37). Indeed, higher BIS showed alpha decreasing (increased cortical activity) compared with higher BAS within the right side (F[1, 61] = 7.77, p ≤ .001, η2 = .35), whereas higher BAS showed a more left alpha decreasing compared with higher BIS (F[1, 61] = 8.50, p ≤ .001, η2 = .39). Secondly, higher BAS showed a more alpha decreasing within the left hemisphere in Experiment 1 more than Experiment 2 (F[1, 61] = 8.56, p ≤ .001, η2 = .37). On the contrary higher BIS showed a more alpha decreasing within the right hemisphere in Experiment 2 more than Experiment 1 (F[1, 61] = 7.75, p ≤ .001, η2 = .36).

E

RTs R R2 β std error t

T

0.41 0.17 0.22 0.15 3.93⁎⁎

C

0.10 0.00 0.28 0.22 0.48

N C O

509 510

b ER R R2 β std error t

3.3.3. Ranking self-perception ANOVA indicated significant effect for group (F[1, 61] = 10.45, p ≤ .001, η2 = .44) and group × experiment (F[1, 61] = 9.17, p ≤ .001, η2 = .40). Firstly, a general high ranking was self-perceived by higher BAS more than higher BIS. Secondly, in Experiment 1 more than Experiment 2 higher BAS showed an increased ranking perception of (F[1, 61] = 10.09, p ≤ .001, η2 = .43). On the contrary in Experiment 2 more than Experiment 1 higher BIS showed a decreased ranking perception (F[1, 61] = 8.16, p ≤ .001, η2 = .39). Moreover, comparing high BAS and high BIS a significant increased ranking perception was found in higher BAS more than higher BIS in Experiment 1 (F[1, 61] = 9.98, p ≤ .001, η2 = .42), whereas a significant decreased ranking perception was found in higher BIS more than higher BAS in Experiment 2 (F[1, 61] = 10.09, p ≤ .001, η2 = .44).

U

507 508

2 for higher BAS (F[1, 61] = 8.10, p ≤ .001, η2 = .39), whereas 527 significant increased RTs were found in Experiment 2 compared with 528 Experiment 1 for higher BIS (F[1, 61] = 8.96, p ≤ .001, η2 = .40). 529

Table 4 Multiple regression for BAS (a) and BIS (b) participants.

t4:4 t4:5 t4:6 t4:7 t4:8 t4:9 t4:10 t4:11 t4:12 t4:13 t4:14 t4:15 t4:16 t4:17 t4:18 t4:19 t4:20 t4:21 t4:22 t4:23 t4:24 t4:25 t4:26 t4:27 t4:28 t4:29 t4:30 t4:31 t4:32 t4:33 t4:34 t4:35 t4:36 t4:37 t4:38 t4:39 t4:40 t4:41 t4:42 t4:43 t4:44 t4:45 t4:46

Q3 t4:3

7

Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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manipulation of the subject's performance has an impact on social rank representation, with a possible direct effect on self-representation. Together, these results suggest that dominance may not be a universally “objective” phenomenon; rather, perception of our own ranking, particularly during conditions of comparison with peers, may be directly and strongly related with personality component. Concerning the significance of the BAS/BIS construct for social status and dominance, we could hypothesize that BIS is associated with negative experience like low-ranking condition, and higher-trait BIS subjects may show to be particularly sensitive to negative and potentially “no-rewarding” condition which may ingenerate negative emotions and submissive attitude. Conversely, higher BAS subjects may be more attentive to conditions that produce a significant positive response and that reinforce the behaviors which are active in nature, ingenerating positive emotions and dominant attitude [3]. Thus, in line with our previous hypotheses, we observed in higher BAS subjects a prevalence in responding to approach condition and conversely in higher BIS subjects a consistent responding to avoidance condition. More generally we have to consider the extent to which individuals of higher social status are more proactive and independent of others in achieving their desired outcomes, as demonstrated for BAS subjects [30]. By virtue of having relatively a greater proactive attitude they must rely more on their resources to meet their needs [27]. This greater level of independency likely leads higher-status individuals to be particularly motivated to be more dominant, thus leading to greater neural (frontal) activity associated with these types of attitudes. This result is consistent with prior research showing that social status is associated with greater BAS during the processing of competitive situations. A second main effect was related to the frontal brain responses to dominance and social status perception. Why might social status relate to neural activity in the frontal network? Prior neuropsychological work has suggested a role for the VMPFC in responding to status cues [26]. Karafin et al. [26] found that patients with VMPFC lesions made less use of information in their dominance judgments. These effects were supported in the present study by modulation of the alpha frequency band, that is, increased brain activity (reduced alpha power) in response to high-ranking perception for BAS, and increased brain activity in response to low ranking perception for BIS. As expected we found that the left side system – more related to BAS polarity – accounts for the increased performance and improved self-perception, as shown by regression analysis. That is, BAS subjects showed a significantly more intense response within the left hemisphere in the case of reinforced dominance in Experiment 1. Conversely BIS subjects revealed a significantly more intense response within the right hemisphere in the case of limited dominance perception. The hemispheric lateralization of cortical effect (more left lateralized for BAS and right lateralized for BIS) suggested a related lateralization effect as a function of attitudinal features of approach-left-response (BAS) and avoidance-right-response (BIS) behavior: the effect of dominance may be supported by the account that BAS may be responsive for active and dominant position whereas BIS may be responsive for avoidant and remissive position [6]. More generally, the results from this study appear to confirm the tendency to modulate both self-perceived social position and real performance based on the personal attitudes (BIS/BAS) and the frontal activity (alpha frequency band) during an inter-personal performance which is considered relevant for social hierarchy. Higher-level hierarchy related to cognitive performance is linked to a clear increased activity in the left frontal side for BAS subjects, when subjects perceived themselves as skillful. By contrast, an increased right side activity for BIS subjects was registered in response to a decreased hierarchy when subjects perceived themselves as low-ranking and less-performing. Moreover, in this study, the regression analysis suggests the frontal brain activity to be predictive of the behavioral and personal perception of social ranking position, since this brain responsiveness is able to determine performance and perceptual modifications. In addition, self-perception and cognitive responses were found to be interconnected. This intrinsic

T

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598 599

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with other people. This effect was paralleled by the behavioral data, related to the real performance. In Experiment 1 higher BAS subjects significantly improved their performance (decreased RTs and ER). This trend was found to be constant during the whole task, with a significant increasing of subjects' attentional ratings. On the contrary, higher BIS showed no relevant effects in terms of increased behavioral performance. That is, they did not show the same significant impact by the external positive and reinforcing feedback during the task. A correlated effect was related to the time variable in Experiment 1. In fact, whereas in the first interval no significant increased performance was detected, from the second interval (after 25 trials) BAS subjects constantly increased their positive performance (for both RTs and ER) during the course of the task. A reverse pattern of behavioral responses was observable in Experiment 2, since subjects with higher BIS showed a significant selfperception of lower social ranking and performed the worst in comparison with the peer group. Indeed they constantly reported a decreased position in their social status and this perception was clearly lower than that expressed by higher BAS subjects. In concomitance, higher BIS produced a poor performance in comparison with higher BAS subjects taking into account both RTs and ER. Overall, higher BAS subjects showed a more reduced effect of the negative ranking condition artificially induced by the experimenter, since they also maintained a generally good performance in Experiment 2. This general, different trend based on the two categories of BIS and BAS participants was reinforced by the time effect. Indeed, a constant increasing of low-level performance and self-perception of low-ranking in higher BIS subjects from the second to the fourth interval was observed, in contrast to the higher BAS subjects who reported a sort of “plateau effect” in Experiment 2. The results observed for both Experiment 1 and 2 are in line with a previous study [16], which reported that those individuals with a higher BAS strength were more likely to relate to the dominant and “propositive” character in situations which were shown to induce a positive effect, while those with a higher BIS sensitivity were more inclined to relate to the submissive and passive character, inducing a negative effect. This raises the possibility that our personalities and our subjective comprehension of social hierarchies may interact to impact our social success and sense of well-being. Furthermore, it is possible that participants implicitly assessed their own (self-referential) social hierarchical status in relation to the task they performed, particularly with respect to social dominance perception. It is also possible that the improved selfperception of ranking (induced by the external feedback) may have introduced a reinforcing cue able to modify significantly behavioral performance [12]. More generally we may suppose that there was a relevant effect related to the impact of perceived performance on cognitive real performance when this rating was compared with that of other similar people. It was found that subjects improved or decreased their real performance (in terms of ER and RTs) in response to the external feedback, that is, the perception of their outcomes in relation with those of the peer group. In comparison with other studies which explored the simple cognitive competencies and their effect on the subjects' social perception, in the present study the social ranking induced by the direct comparison with other similar subjects introduced a relevant hierarchy effect. That is, the social significance of the performance for the hierarchy status appears to be highly relevant in modulating the subjects' performance across the task, as it was also reported by the subjects in the postexperiment questionnaire. This effect was observed for the entire duration of the experiment with a consistent and constant increasing (in case of perceived improving) or decreasing (in case of perceived decreasing) of the cognitive outcomes. In this regard Festinger's longstanding, prominent theory of social comparison processes [18] suggested an important role for hierarchical rank in achieving accurate self-knowledge, self-representation and self-improvement, particularly in the usage of upward social comparisons, that is, comparisons between oneself and an individual of high/low status. Therefore the

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Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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The paper was supported by Catholic University Found D 1.1 2013.

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relationship also highlights the possibility of considering the reciprocal influence of cognition and self-perception as two sides of the same coin. Given the evolutionary prevalence and importance of social dominance hierarchy across species and across human social groups, it is plausible that the “social” brain has specialized mechanisms for perceiving hierarchy and dominance in integration with specific personality factors. The current research provides initial evidence for this hypothesis and lays a foundation for future research examining the extent to which the human brain selectively processes social dominance cues. The present studies represent an important step in understanding how social status influences neurocognitive processes related to navigating the social world. However, the experiments are not without limitations. First, it is necessary to consider the specific context where the social ranking effect was analyzed, that is, the fact that subjects did not directly see their “competitor”. Indeed, an indirect comparison was produced, by communicating to the experimental subjects that their performance was constantly compared with those of other similar young participants. Perhaps a more direct (visible) competitor could induce different emotional (perhaps also more accentuated) responses and probably higher overt facial displays. Secondly, the effect of “mixed profiles” based on BAS and BIS constructs may better elucidate the contribution by the two components, by pointing out the “integration effect” of both of them. Finally, different experimental contexts may be introduced to explore the dominance construct independently from the cognitive, competitive ranking induced by the present experiments. That is, for example, a more cooperative condition may be included, where a bottom- (less dominant) and a top-level (more dominant) of dominance is finalized to create a supportive relationship between people.

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Please cite this article as: Balconi M, Pagani S, Personality correlates (BAS-BIS), self-perception of social ranking, and cortical (alpha frequency band) modulation in peer-group comparison, Physiol Behav (2014), http://dx.doi.org/10.1016/j.physbeh.2014.05.043

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