Empathy refers to a complex construct that plays a key role in social adaption and quality of human relationships. It includes the capacity of sharing emotions and responds immediately to the emotions of others (affective empathy) and the ability to understand what other people are thinking, imputing desires, and intentions to oneself and others (cognitive empathy) close to the concept of the theory of mind (ToM) (Decety and Jackson, 2004; Decety and Moriguchi, 2007; Young et al., 2007; Blair, 2008; de Waal, 2008). Several studies showed that ToM deficits in a variety of psychiatric disorders including autism, schizophrenia, bipolar disorder, and attention-deficit/hyperactivity disorder (Corcoran et al., 1995; Kerr et al., 2003; Abikoff et al., 2004; Blair, 2005; Bora and Pantelis, 2016; Maoz et al., 2019). There is a wide agreement that adult humans are able to engage in unconscious analyses of others’ mental states in the context of automatic perspective taking (Samson et al., 2010; Low and Watts, 2013; Surtees et al., 2016; Schneider et al., 2017). This human ability may be of key importance for the mostly unconscious ascription of mental states needed for social interactions such as cooperating with colleagues and family members, thinking about others in their absence and anticipating their emotional reactions. The psychological mechanisms surrounding this ability remains, however, matter of intense debate. Recent lines of evidence suggested the idea that ToM is controlled by two distinct systems: one explicit that deliberately considers other’s thoughts and emotions and one implicit based on the automatic analysis of their viewpoints even when such analysis is irrelevant for task processing (Onishi and Baillargeon, 2005; Surian et al., 2007; Kovacs et al., 2010; Schneider et al., 2012b). Supporting this viewpoint, infants in the second year of life appear to represent others’ false beliefs when tested using implicit looking time measures (Onishi and Baillargeon, 2005; Kovacs et al., 2010), despite their poor performances on false belief tests that require explicit, verbal responses until 4 years of age (Wellman et al., 2001). In the same line, patients with autism spectrum disorder show less evidence of implicit mentalizing than neurotypical individuals, although both neurotypical and neuro-atypical individuals perform similarly on explicit verbal ToM tasks (Senju et al., 2009; Schneider et al., 2013). Other researchers argued against this distinction and proposed that domain-general attention cueing and executive functions may explain automatic perspective taking (APT) without specificity for social stimuli (for review see Cole and Millett, 2019; Westra et al., 2021).

Neurotypical adults are prone to systematic difficulties arising from conflict between their own (self) and another’s (other) perspective. Some observations suggested that adult participants show “egocentrism” across a wide range of tasks in that their judgment of what someone else sees, are slower or more error prone when this differs from what participants themselves see (Qureshi et al., 2020). This gives rise to the widely reported phenomenon of “egocentric bias” toward the participant’s own perspective, which is almost universally observed in studies of ToM (Royzman et al., 2003; Wellman, 2014). Much of the debate regarding implicit mentalizing concerned the experimental results on the dot perspective-taking task (dPT), originally developed by Samson et al. (2010). In this task, participants are asked to count the number of dots on a screen. Importantly, an avatar is also present on the screen when the dots are revealed and sees a number of dots that is either the same as (consistent trials) or less than the number of dots that the participant sees (inconsistent trials). As expected and consistent with the notion of egocentric interference, participants take longer to report the number of dots the avatar sees when the number of dots the participant sees is different. However, participants also take longer to report how many dots they themselves see when the avatar sees a different number of dots. This second form of error was characterized as altercentric interference: participants’ ability to report their own perspective is affected by the perspective of the avatar (Qureshi et al., 2010; Samson et al., 2010). Despite the uncertainties about the specificity of the psychological mechanisms surrounding egocentric and altercentric interference, there is no doubt that these parameters may impact on social interactions both in general population and clinical samples (Furlanetto et al., 2016; Drayton et al., 2018; Gao et al., 2019; Del Sette et al., 2022). As an example, compared to younger persons in dPT, individuals older that 55 years show an increase sensitivity to other’s conflicting viewpoint as documented by increased reaction time in case of incongruence when adopting their own perspective (Martin et al., 2019).

The brain substrates of dPT and in particular egocentric and altercentric interference are complex and remain matter of intense debate. Early functional MRI (fMRI) observations showed an activation of the dorsolateral prefrontal, parietal cortices when selecting one’s own over another’s visual perspective, and vice versa mainly in case of conflict between the two perspectives (Ramsey et al., 2013). In the same line, a domain-specific activation in several cortical areas such as right temporo-parietal junction and ventral medial prefrontal cortex was described in inconsistent trials when selecting one’s own perspective (Schurz et al., 2015), although this position has been also challenged (Santiesteban et al., 2017). The right temporo-parietal junction stimulation significantly improved the judgment from the allocentric perspective, whereas stimulation of the dorsomedial prefrontal cortex improved performance from the egocentric perspective (Yao et al., 2021). Using transcranial direct current stimulation during a visual perspective task, (Martin et al., 2017) also reported a key role of dorsomedial prefrontal cortex in the integration of external information when adopting the self-perspective. In a meta-analysis of fMRI findings, (Arora et al., 2017) stressed the paucity of fMRI studies focusing on dPT and reported no consistent overlap of dPT activation patterns with the ToM core regions.

Besides limited samples and absence of concomitant consideration of Self versus Other and Consistent versus Inconsistent effect on brain activation, one main limitation of these studies is that they did not take into account cognitive and emotional parameters that, at an individual level, impact on the expression of APT in humans such as attention processing, inhibitory control, but also social cognition (Schneider et al., 2012a; Burnside et al., 2017; Pineda-Alhucema et al., 2018). More recently, it has been reported that people with lower attentional resources and decreased inhibitory control [measured with the Conner’s Continuous Performance Test-II (CPT-II)] display worse performances in the dPT task and make more errors when judging conflicting perspectives both according to their own and other viewpoints (Rodriguez et al., 2022). However, this latter study concerned only clinical observations without reference to dPT-related brain activation patterns. The present report aims to explore whether psychological variables characteristic of each individual determine the brain reactivity in dPT. Our hypothesis was that the level of fluid intelligence, regulation of attentional resources and inhibitory control but also identification and expression of emotions as well as ToM global performance might impact on the activation of neural generators needed to deal with conflicting views when judging our own versus other’s perspective. This fMRI study explores differences in individual z-scores (rather than group differences in patterns of brain activation) in eighty-two healthy adults who underwent a detailed assessment of fluid intelligence, attention, levels of alexithymia and social cognition abilities prior to the administration of the Samson’s dPT. Taking into account the previous contributions in this field (Schneider et al., 2012a; Kanske et al., 2015; Burnside et al., 2017; Pineda-Alhucema et al., 2018; Rodriguez et al., 2022) we expected that deficits in attention and inhibitory control would be associated with increased egocentric and altercentric interference-related BOLD signal. We also postulated that decreased abilities in the recognition of emotions and ToM would increase brain reactivity to egocentric interference.

To our knowledge, this is the first study attempting to explore at an individual level the impact of cognitive and emotional parameters on the activation of human brain during automatic perspective taking. Individual fMRI z-scores when focusing on Self perspective depend on the levels of fluid intelligence. Among cognitive parameters, decreased attentional recruitment and decreased inhibitory control is related to lower fMRI z-scores when adopting the Other’s perspective. Brain activation associated with egocentric interference was significantly lower in cases with better empathy abilities but significantly higher in persons with higher levels of alexithymia (implying increased difficulties in the recognition of emotions).

The association between fluid intelligence measures and fMRI z-scores concerned only the Self condition in the present series. In other words, persons with higher levels of intelligence display increased brain activation when focusing on their own perspective. The increased recruitment of neural resources in the Self condition among persons with higher WAIS scores is consistent with several fMRI articles showing stronger brain activity (mainly in frontoparietal networks) in the presence of higher fluid intelligence in sleep, resting state and following activation with a variety of cognitive paradigms (Gray et al., 2003; Fang et al., 2019, 2022; Assem et al., 2020; Santarnecchi et al., 2021). Brain activation in our experimental setting does not depend on the levels of attention and inhibitory control (as measured by CPT-II parameters). Intriguingly, the effect of fluid intelligence on fMRI z-scores was not found when taking the Other’s perspective. In this situation, individuals with decreased attention and inhibitory control (independently of their WAIS performances) displayed lower fMRI z-scores. Earlier studies reported that attentional orienting contributes decisively to performance in the dPT (Bukowski and Samson, 2017; Gardner et al., 2018). In our recent behavioral analysis using the same experimental paradigm, it has been shown that people with decreased levels of attention and decreased inhibitory control may need more time and make more errors when judging the Other’s perspective (Rodriguez et al., 2022). Extending these observations by adding fMRI data, our results imply that, compared to the Self condition, the brain activation needed for taking the Other’s perspective is more difficult to sustain in the presence of lower attentional resources and decreased inhibitory control. Taken together, these findings reveal a dissociation between the psychological factors that may determine brain reactivity during perspective taking. The level of fluid intelligence contributes to individual differences in brain activation in “Seeing it on my way” condition. In “Seeing it on the Other’s way” condition, these latter depend, at least partly, on preserved attention and inhibitory control.

One main focus of the present study was the analysis of the determinants of brain activation associated with altercentric versus egocentric interference. The individual fMRI z-scores for the Self Inconsistent-Self Consistent contrast (altercentric interference) as well as for the Other Inconsistent- Other Consistent contrast (egocentric interference) reported here provide a fMRI correlate of these interferences. In our models, the fMRI z-scores associated with altercentric interference were not related to fluid intelligence, attention, social cognition, and levels of alexithymia. An opposite scenario is present for the egocentric interference. The fMRI z-scores for this contrast are higher in cases with worst abilities of social cognition. This observation extends earlier behavioral reports by Bukowski and Samson (2016) and Mattan et al. (2016) who reported that lower levels of empathy and negative emotions are associated with higher interference in case of conflicting perspective. Altogether these observations imply that, from an imaging standpoint, the “egocentric” bias when adopting the Other’s perspective could be more pronounced in persons less able to deal with emotional challenges and decreased abilities in theory of mind and affective empathy.

The present data suggest that neurocognitive and psychological attributes should be taken into account when interpreting the individual differences of brain activation in dPT. The fact that distinct cognitive and emotional parameters impact on fMRI z-scores related to Self and Other perspective but also altercentric and egocentric interference should be interpreted within the theoretical framework of the link between emotional regulation, cognition and ability to take other’s perspective. Most previous reports in this field concerned clinical populations. The dPT performances may be preserved in psychiatric pathologies affecting intelligence but also emotional regulation such as autism spectrum conditions and alcoholism (Pearson et al., 2013; Cox et al., 2016; Sijtsma et al., 2020). In contrast, they are known to be affected in patients with attention deficits syndrome (Nilsen et al., 2013). High levels of egocentric interference has been also reported in narcissistic personality (Bukowski and Samson, 2021) whereas lower performances in dPT were found in patients with mixed personality and anxiety disorders (Czekoova et al., 2020; Shaw et al., 2020). In the present study of healthy controls, decreased fluid intelligence, levels of attention and inhibitory control but also worst identification and expression of emotions as well as decreased social cognition abilities impact negatively on brain reactivity during dPT. To date, no fMRI data are available to explore whether these observations are valid in clinical samples. It would be thus of interest to investigate the fMRI z-scores in prodromal and mild cases with deficient inhibitory control such as obsessive-compulsive disorder (Mancini et al., 2018), primary motor stereotypies (Mirabella et al., 2020), autism spectrum disorder (Schmitt et al., 2018), Parkinson’s disease (Di Caprio et al., 2020), and attention-deficit/hyperactivity disorder (van Hulst et al., 2018).

The strengths of this report include its use of a large sample, independent variables assessing cognitive processes such as attention and fluid intelligence, general levels of empathy, but also inhibitory control and stringent control for multiple comparisons in the regression models. Some limitations should also be noted. Conceptually, one should keep in mind that APT is one among the facets involved in social cognition. For some authors, the unconscious impact of other’s divergent viewpoint when we focus on our own visual experience is mostly driven by the activation of self-other distinction, self-updating via integration of self-relevant information, central executive functions and mirroring (Bukowski, 2018; Alcala-Lopez et al., 2019). Our data did not address the correlations between these cognitive dimensions and brain reactivity. In the same line, the present findings concern only the Samson’s dPT and are not applicable to ToM paradigms involving how the objects and their arrangement may look to another person. All of our cases were socially integrated young men without history of criminal convictions and substance abuse who were initially recruited as part of a study focusing on psychopathy in the context of forensic psychiatry. The absence of women as well as the careful exclusion of neurological and psychiatric disorders as well as regular use of psychotropics, as well as scores of all of the cognitive and emotional variables within the normal range limit the generalizability of our observations. Studying dPT-related patterns of fMRI activation in persons with clinically overt learning and attention deficits as well as disorders characterized by high levels of alexithymia and decreased abilities of social cognition such as antisocial and schizoid personality (including Asperger syndrome) could be of particular interest in the current effort to define diagnostic and prognostic markers for these conditions.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Commission Cantonale d’Éthique de la Recherche (CCER). The patients/participants provided their written informed consent to participate in this study.

PG, SH, AP, and M-LM: study conceptualization. M-LM: conceptualize the visual perspective-taking task. CR and M-LM: recruitment. M-LM, CR, and PG: neuropsychology supervising. M-LM and FH: data preparation. M-LM, FH, and PG: analyze the data. PG, FH, M-LM, and SH: manuscript writing. All authors contributed to the article and approved the submitted version.