Frontal Alpha Asymmetry Reveals a Relationship Between Human Approach Motivation and the Propensity to Take the Altercentric Perspective

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Frontal Alpha Asymmetry Reveals a Relationship Between Human Approach Motivation and the Propensity to Take the Altercentric Perspective

https://doi.org/10.21203/rs.3.rs-4962788/v1

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Frontal asymmetry in the EEG alpha frequency allows to distinguish greater left activation relating to approach motivation from greater right activation relating to withdrawal motivation. It has been mostly studied in the context of affective empathy. Instead, it remains unknown whether it can be specifically related to one key component of the cognitive dimension of empathy, i.e., visuospatial perspective-taking (VSPT). In the present study, we intended to bridge this gap. To this aim, we administered an implicit VSPT task in which participants were presented with scenes of an agent grasping an object, gazing at it, or both, or neither, and were required to judge the left/right location of the object, without receiving any instruction about the perspective to take. The same participants underwent a resting state EEG recording to obtain an index of frontal alpha asymmetry. Correlational analyses showed a positive relationship between left frontal activation and the spontaneous tendency to take the agent’s perspective (altercentric propensity) when the agent behaved ambiguously, grasping the object while not gazing to it. These results suggest that the onlooker’s spontaneous altercentric propensity implies the approach motivation in the effort to understand what another individual is intending to do.

visuospatial perspective-taking

frontal alpha asymmetry

social cognition

empathy

altercentrism

The approach-withdrawal model of hemispheric activation [1, 2] posits that left frontal cortical areas mediate approach motivation, whereas right frontal cortical areas mediate withdrawal motivation. This model largely relies on measures of frontal asymmetry in the EEG alpha frequency range classically used as a proxy to humans’ emotional-motivational tendencies [3, 4]. The frontal alpha asymmetry (FAA) indicates the difference in electrical activity, in terms of alpha power, between the frontal regions of the two hemispheres. A higher value of asymmetry (i.e., the result of the difference between F4 and F3) indicates higher cortical activity in the left frontal region, whereas a lower value of asymmetry suggests higher right frontal activity [3, 4]. Thus, the finding of greater left activation (i.e., higher or positive FAA score) relating to the approach motivation toward stimuli and greater right activation (i.e., lower or negative FAA score) relating to the withdrawal motivation from stimuli supported the view that FAA can be considered a marker of these two opposite human tendencies [1–4].

Approach versus withdrawal motivation is a key construct in the field of social cognition, and several studies investigated the relationship between FAA and social cognition skills such as empathy. Two main components of empathy have been distinguished. Affective empathy, as defined by Lawrence [5], refers to the degree to which an individual experiences others’ feelings, whereas cognitive empathy refers to the capacity to adopt another’s perspective to understand another’s thoughts, intentions and beliefs [6, 7]. Affective and cognitive empathy are considered to be at least partially dissociable constructs [8, 9]. In the affective domain, significant relationships have been observed between FAA and empathy but with contrasting results [10–13]. Indeed, since left FAA is associated to approach motivation and because empathy can be seen as an inclination towards closeness with others, it has been postulated that affective empathy should be related to left frontal asymmetry [14, 15]. However, some evidence found a correlation between right FAA and empathic responses [10, 13], suggesting that empathy could represent a selfish impulse to alleviate one’s own sadness when perceiving it in others, thereby promoting withdrawal tendencies [13]. At the present, no data are available to establish whether and how FAA relates to cognitive empathy.

One key aspect of the cognitive empathy is visuospatial perspective-taking (VSPT) [7, 16–18], defined as “any process by which one infers something about the visual or spatial properties of a scene in relation to another person or position” [19]. Indeed, people are capable of perceiving and judging a situation from different points of view [20]. These include the egocentric perspective, which is the way the situation is perceived and judged from the individual’s own perspective, and the altercentric perspective, which is the way the situation is perceived and judged from the perspective of another person involved in the situation [21–26]. Some studies have found the primacy of the egocentric frame of reference (i.e., egocentric bias) [22, 24]. Nonetheless, a shifting towards an altercentric point of view can occur even spontaneously while performing VSPT tasks [27–31].

The aim of the present study was to test whether the tendency to spontaneously assume another’s point of view, i.e. altercentric propensity, is related to the approach motivation or to the withdrawal one, as revealed by FAA. The controversial data on the way in which FAA relates to affective empathy suggest caution in intuitively implying that the altercentric propensity could be related to approach motivation. Indeed, one could expect the altercentric propensity would imply a willingness to interact with another agent [32], thus being correlated with left FAA characterizing the approach motivation. However, as recalled above, studies showing that affective empathy correlates with right FAA [10, 13], might lead to expect that cognitive empathy too is related to withdrawal tendencies.

To address this issue, we used an implicit VSPT task, developed by Mazzarella et al. [29], requiring participants to judge the location of a target object placed in a scene in which an agent is present; the participants can spontaneously adopt their own or the agent’s perspective since task instructions do not explicitly require to choose a specific viewpoint. Relevantly, the agent interacts with the target through different cues: grasping the object, gazing at it, or both, or neither grasping nor gazing at the object. By this means it is possible to test whether, and with which cue, the agent’s behaviour makes participants more likely to adopt an altercentric perspective. Indeed, observing an agent interacting with a target object, such as by grasping or gazing at it, can differently promote the processing of the agent’s perspective in order to facilitate understanding another’s behavior [27–30].

Here, by using this implicit VSPT task we could test whether FAA is specifically related to different agent’s cues affecting the participants’ spontaneous altercentric propensity.

Participants

To identify a target sample size adequate to test the relationships between FAA and VSPT, an a priori power analyses was conducted (g*power) [33]. Given that a large effect size has been shown to be adequate for identifying effects of interest in frontal alpha asymmetry research [10], a sample of 28 participants is necessary to ensure detecting an effect of critical interest with a power of 0.90 at an alpha level of 0.05 with a large effect size (i.e., .50) in correlational analyses.

A total of 34 participants (14 females; mean age: 24.64 ± 3.20, range 18–30) was recruited from University of Campania ‘Luigi Vanvitelli’ (Southern Italy) for this study. Three participants were excluded due to bad EEG recordings. The final sample consisted of 31 right-handed healthy participants (13 females; mean age: 24.32 ± 3.16, range 18–30), free from psychiatric, neurological or other medical conditions. The study was approved by the Ethics Committee of the Department of Psychology of the University of Campania ‘Luigi Vanvitelli’ and conducted in accordance with the ethical standards of the Helsinki Declaration. Written informed consent was obtained from all participants before the experimental procedure.

VSPT task

The VSPT task was performed following the same paradigm as in previous studies [27, 29]. Participants were presented with black and white scenes representing a human agent (an actress) seated behind a table on which one target object (a bottle) was positioned. Four scenes were used (Fig. 1 provides the images of the actress who actually posed for the experiment. She is the corresponding author of the manuscript, and she agrees to be published in the image). In the first scene the actress gazed and grasped the bottle (yes-gaze/yes-action). In the second scene she gazed towards the bottle but did not grasp it (yes-gaze/no-action). In the third scene she did not gaze the bottle but only grasped it (no-gaze/yes-action). In the fourth scene she did not gaze or grasp the bottle (no-gaze/no-action). In both yes-gaze conditions the actress fixated precisely the point in which her hand would have come into contact with the target object. The scenes were mirrored in such a way that the target object was positioned on either side of the agent (total number of stimuli = 8). Each scene was enclosed in a rectangular frame in a 700 x 500-pixel array. In each trial, a fixation point (800 ms) was followed by a scene that remained on the screen until participants’ response.

Before starting the experimental session, participants were presented with instructions, which required a left/right coding of the bottle location without making any mention about the perspective to assume. The instructions were the following: “Where is the bottle? To the left or to the right?”. Participants were required to press “B” for left and “H” for right on a QWERTY keyboard with their right dominant hand. Each scene was repeated six times in a randomised order (total number of trials = 48). Four additional random trials with the same stimuli used in the experimental session were presented in a practice session and discarded from statistical analysis.

Participants’ left and right responses and reaction times were recorded. Since in previous studies the number of participants’ left and right responses but not the reaction times were differently affected by the experimental conditions [27, 29, 34, 35], here we analysed participants’ responses only (see Statistical analysis section).

EEG data recording and preprocessing

Scalp EEG signals were acquired using a 32-channel EMOTIV EPOC headset (Emotiv©, San Francisco, USA). The acquisition procedure employed 32 electrodes, Cz, Fz, Fp1, F7, F3, FC1, C3, FC5, FT9, T7, CP5, CP1, P3, P7, PO9, O1, Pz, Oz, O2, PO10, P8, P4, CP2, CP6, T8, FT10, FC6, C4, FC2, F4, F8, Fp2, and reference, TP9 and TP10, in accordance with the 10–20 International System (Fig. 2). The sampling rate was 128 Hz and EEG recordings were acquired by the software EMOTIV Pro (Emotiv©, San Francisco, USA). The electrodes were moistened with a saline solution in order to enhance adhesion to the skin and optimize the quality of the recording. During EEG acquisition the participants were instructed to remain still with their eyes closed for a period of six minutes, following Tomarken et al.’s [36] guidelines.

Data preprocessing was performed using EEGLAB [37]. EEG data were resampled to 256 Hz and re-referenced to the average of the activity. Data were then band-pass filtered between 0.5–40 Hz to remove high frequencies due to artifacts and signal contamination. Then, Independent Component Analysis (ICA) was applied to enhance artifact correction. Since we were interested in alpha activity, data were divided into standardized frequencies, delta (0.5-4 Hz), theta (4–8 Hz), alpha (8–12 Hz), and beta (12–35 Hz). In the present study, only alpha frequencies were analysed. Previously removed bad channels were interpolated using the linear interpolation method. Given our interest in frontal alpha asymmetry, the Fast Fourier Transform (FFT) was applied to obtain the alpha signal on the following channels: F3, F4, P3, and P4. In particular, the difference between the frontal channels (F4F3) was computed to obtain the FAA index [38]. Additionally, a non-frontal alpha asymmetry index was calculated as a control variable using the difference between two parietal channels (P4P3) [13]. Since the alpha signal (8–12 Hz) is inversely associated with cortical activity [39], higher or positive values of FAA are indicative of a stronger left hemispheric activation, while lower or negative values of FAA are indicative of a stronger right hemispheric activation.

Procedure

Before starting the experiment, participants were informed that they could communicate to the experimenter any issues or concerns that arose during the study and could withdraw at any time.

In the first phase of the study we administered the VSPT task, created by OpenSesame software [40] and implemented on JATOS, an online study administration platform [41]. The online administration was conducted via video call with the experimenter, who remained available to address any queries the participants might have. This phase lasted approximately 10 minutes. Thereafter, within a week after the first phase, the EEG recording session was held at the laboratories of the University of Campania ‘Luigi Vanvitelli’.

Statistical analysis

Preliminary descriptive analyses were carried out to examine missing values and variable distributions. Shapiro-Wilk tests were conducted to assess the normality of the dataset for the two alpha asymmetry index (FAA and Control) and the mean of altercentric responses in the four conditions of the VSPT task. No variable was distributed normally (all p < .001).

For the purposes of the analysis, participants’ left and right responses on the VSPT task were transformed into a binary code: those consistent with an egocentric perspective were scored as 0, whereas those consistent with an altercentric perspective were scored as 1 [29]. Values deriving from this binary coding were arcsine transformed for performing parametrical statistical analysis [42]. Thus, a 2x2 repeated-measures ANOVA could be carried out on the mean of altercentric responses, with action (yes/no) and gaze (yes/no) as within-subject factors [29].

Spearman’s rank correlations (r_s) were used as the appropriate statistical analysis, due to the violation of normality. Spearman’s rank correlations (r_s) were executed on the mean of altercentric responses in the four VSPT task conditions (yes gaze/yes action, yes gaze/no action, no gaze/yes action, no gaze/no action) and the two alpha signals: FAA index (F4F3); Control index (P4P3). Statistical analyses were performed using the Statistical Package for Social Sciences (SPSS Inc., version 25).

Descriptive analyses regarding the four conditions of the VSPT task and the alpha signal are reported in Table 1. Results of the ANOVA on participants’ responses on the VPT task showed no significant main effects of the agent’s action, F(1,30) = .151, p = .700, h²_p = .005, or gaze, F(1,30) = 2.366, p = .135, h²_p = .073. The action by gaze interaction was not statistically significant, F(1,30) = .245, p = .624, h²_p = .008.

Table 1

Descriptive statistics.
Variables	Mean	Min	Max	Skewness	Kurtosis
1. Frontal Asymmetry	-1.09 (1.19)	-4.94	− .02	-1.76	3.14
2. Control Asymmetry	.25 (.62)	− .71	2.62	2.2	6.5
3. No gaze/no action	.11 (.28)	0	1	2.65	5.91
4. Yes gaze/no action	.14 (.28)	0	1	2.32	4.49
5. No gaze/yes action	.12 (.28)	0	1	2.42	4.82
6. Yes gaze/yes action	.13 (.28)	0	1	2.38	4.92

1. Frontal Asymmetry: Frontal Alpha Asymmetry (F4F3); 2. Control Asymmetry: Parietal Alpha Asymmetry (P4P3); 3–6: the four VSPT task conditions.

Spearman’s rank correlation coefficients (r_s; Table 2) showed significant positive correlations among the altercentric responses on the VSPT task conditions, and a significant negative correlation between alpha asymmetry on the frontal and the control (parietal) location. More relevant here, a significant positive correlation was found between FAA index and the no gaze/yes action condition (p = .023), indicating a positive relation between left frontal activation and altercentric responses in this condition of the VSPT task, while no other significant correlation was found between alpha asymmetry and altercentric responses on the remaining task conditions (Fig. 3).

Table 2

Spearman’s correlations.
Variables	1	2	3	4	5	6
1. Frontal Asymmetry F4F3	-
2. Control Asymmetry P4P3	− .500**	-
3. No gaze/no action	.166	− .014	-
4. Yes gaze/no action	.133	.077	.643**	-
5. No gaze/yes action	.407*	− .240	− .728**	.707**	-
6. Yes gaze/yes action	.280	− .085	.839**	.707**	− .705**	-

1. Frontal Asymmetry: Frontal Alpha Asymmetry (F4F3); 2. Control Asymmetry: Parietal Alpha Asymmetry (P4P3); 3–6: four VSPT task conditions. *p < .05; **p < .01; ***p < .001.

Searching for relationships between FAA and the ability to take another’s point of view, we observed that participants with higher FAA scores, i.e., stronger left frontal activation, tended more to spontaneously adopt another’s point of view. This result suggests that the spontaneous altercentric propensity may imply the individual’s approach tendency towards the agent whose perspective is adopted. Importantly, FAA was significantly related to the VSPT condition in which the participants observed the agent grasping the bottle while not gazing to it. This finding indicates that the approach tendency towards the agent in a VSPT scenario might be particularly activated when the agent provides a specific combination of cues, making the agent’s intention ambiguous. Indeed, viewing an agent reaching for a target without looking at it may be perceived as ambiguous, since gaze and action do not carry the same information about the agent’s behavioral intention [28]. Such an ambiguity does not occur when observing an agent only gazing towards the target (but not grasping it) or when the agent congruently gazes and grasps the object [27, 30]. In two implicit VSPT experiments, Furlanetto et al. [28] investigated the effects of the agent’s action and gaze on the altercentric propensity. The former experiment showed that the more the actor was perceived as potentially interacting with the objects, as revealed by convergent action and gaze cues towards the to-be-coded object, the stronger the tendency to take his perspective. However, the latter experiment demonstrated that such altercentric tendency even increased when gaze and reaching information was incongruous, i.e. when the agent grasped the object while looking straight ahead, making the agent’s behavioral intention ambiguous. These findings supported the idea that spontaneous perspective-taking is involved in action understanding [27, 30]. When the agent’s action is more difficult to understand, there is a stronger tendency to take her/his perspective to better understand what she/he is intending to do. Such a situation corresponds to the ambiguous condition of the present VSPT task, i.e., yes action/no gaze, in which we observed the significant correlation with FAA. Furlanetto et al.’s [28] results reconcile previous findings from studies investigating the relative contribution of gaze and action cues to perspective-taking [29, 30] suggesting that the agent’s action but not eye gaze favoured the altercentric perspective. Indeed, rather than depending on specific cues (and not others), VSPT seems to be influenced by the extent to which patterns of cues convey attribution of intentions to others.

It is worth underscoring here that in the present study we did not find significant main effects of the agent’s action and gaze nor an interaction between the two cues on the number of participants’ altercentric responses, at variance with the previous VSPT experiments using the same task [29]. However, although in the present study we adopted the same VSPT paradigm as in Mazzarella et al. [29], the stimuli differed since a different agent was placed in the present VSPT scenario. This might not be a trivial issue, since a growing amount of data highlighted that individual disposition to take another’s perspective might depend on several factors, including features of the observed agent [23, 27, 43]. Nonetheless, here we observed a specific positive relationship between FAA and the altercentric propensity in the yes action/no gaze condition. Thus, our results supported the interpretation that spontaneous altercentric propensity implies approach motivation. These findings are consistent with results of a transcranial direct current stimulation (tDCS) study by Conson et al. [35] demonstrating that concurrent facilitation of right and inhibition of left lateral prefrontal cortex interfered with the altercentric propensity in a VSPT task. In that study the authors also compared the effects of the stimulation on the VSPT task and on a task requiring recognition of emotional faces; the findings showed that tDCS speeded-up only responses to threatening faces, consistent with data showing dissociation between cognitive and affective components of empathy [8, 9]. Indeed, as recalled above, right FAA and the implied withdrawal motivation have been found related with affective empathy [10, 13]. Two main reasons might account for differences between the present results and the data on affective empathy. First, previous research suggested that emotional processes, involved in affective but not cognitive empathy, contribute most to the asymmetry index [4]. Second, our behavioral paradigm testing VSPT did not explicitly require participants to assume another’s point of view, whereas studies on affective empathy tend to explicitly require participants to engage themselves in processing another’s point of view [10, 13]. The explicit vs. the implicit nature of the task could be a relevant factor, as it affects the processes involved in VSPT, with a stronger recruitment of domain-general executive functions, subserved by prefrontal cortex, when the task explicitly requires taking another’s perspective [22, 44, 45]. This aspect could be an important methodological variable to consider in future studies testing relationships between FAA and different components of empathy.

Some limitations of the present study need to be discussed. First, our sample included young adults aged 18–30 years. As existing literature indicated that FAA is a stable measure in time [46, 47] whereas cognitive empathy declines across the lifespan, particularly in older adults [48, 49], we cannot generalize our findings of a correlation between left FAA and the propensity to assume another’ perspective. Future studies should consider a longitudinal design or a wider participants’ age range. Second, we did not evaluate participants’ individual differences on personality traits likely interacting with perspective-taking [19] and, more broadly, with social cognition skills [50–54]. Therefore, further investigations are necessary to comprehend the impact of those traits on the relationship between left FAA and altercentric propensity.

Notwithstanding the above limitations, the present data support the hypothesis that a relationship exists between approach motivation and the altercentric propensity, especially in contexts where a person is facing a situation in which another person provides ambiguous signals not allowing the onlooker to infer her/his intentions immediately. In such conditions the approach motivation could prompt the onlooker to abandon own, egocentric, perspective and “move” towards the altercentric one in the effort of decoding another’s signals and intentions.

Author contributions

I.Z. co-designed the study and wrote the first draft. R.C. conducted the analysis and wrote the first draft. A.L., A.E. and G.C. managed the data collection and conducted the analysis. L.T. edited the manuscript. M.A., R.N. and A.R. collected the data. M.C. co-designed the study, wrote the first draft and edited the manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Correspondence and requests for materials should be addressed to the second author (R.C).

Data availability

Requests for materials and data should be addressed to the second author (R.C).

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Frontal Alpha Asymmetry Reveals a Relationship Between Human Approach Motivation and the Propensity to Take the Altercentric Perspective

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Introduction

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VSPT task

EEG data recording and preprocessing

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