Reexamining empathy in autism: Empathic disequilibrium as a novel predictor of autism diagnosis and autistic traits (2024)

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Abstract

Keywords: cognitive, empathy, autism, emotional empathy, empathy, response surface analysis

BACKGROUND

Autism is a common neurodevelopmental condition and is characterized by marked social difficulties, especially in communication (American Psychiatric Association, 2013). The difficulty in communicating may partially explain why many autistic individuals are vulnerable to exclusion, show high rates of mental health difficulties including depression and anxiety, and often report feeling misunderstood by others (Camm‐Crosbie et al.,2019; Lever & Geurts,2016; Maddox et al.,2017).

These difficulties in communication have often been studied as reflecting empathy deficits (Decety & Moriguchi,2007); yet such conceptualization is sometimes at odds with autistic individuals' accounts (Gillespie‐Lynch et al.,2017). Therefore, there is a need to understand empathy in autism. Many studies show that autistic individuals are characterized by deficits in cognitive empathy (recognizing another person's mental states) alongside intact emotional (or affective) empathy (responding to another person's mental states with an appropriate emotion) (Baron‐Cohen,2013). Other studies find that some autistic individuals show typical cognitive empathy and some even report an excess of emotional empathy (Gillespie‐Lynch et al.,2017; Lombardo et al.,2016). This suggests that ‘deficits’ in empathy do not accurately reflect autistic individuals' empathy abilities. It is therefore important to examine how the two empathy components interact. The concept of empathic disequilibrium, that is, the tendency to experience relatively higher emotional than cognitive empathy (or vice versa) reflects the relationship between the two components, and is associated with autistic traits in the typical population, above and beyond overall empathy (Shalev & Uzefovsky,2020). In the current study, we examined whether empathic disequilibrium is also associated with an autism diagnosis.

Empathy is the ability to understand another's mental states and respond to these with an appropriate emotion (Decety & Jackson,2004). Empathy can be separated into an emotional and a cognitive component. Emotional empathy (EE), also called affective empathy, is the ability to respond to another's mental state with an appropriate emotion, and cognitive empathy (CE) is the ability to recognize what another person is thinking or feeling (Baron‐Cohen & Wheelwright,2004).

The two empathy components are rooted in distinct yet interrelated neurobiological evolved mechanisms and have different developmental, neural, and genetic trajectories. From a developmental perspective, EE appears very early in life and remains stable or increases slightly during the second year of life (Knafo et al.,2008). Conversely, CE develops later in the first year of life and increases throughout life.

A recent meta‐analysis of twin studies (k=23; Abramson et al.,2020) revealed that the dissociation between EE and CE is also supported at the genetic level with EE more influenced by heritability than CE (estimated 48.3% for EE and 26.9% for CE), and CE, unlike EE, depending on shared‐environment (Abramson et al. suggested that cultural norms and beliefs about emotions were possible shred‐environmental factors). There is some indication that the difference in heritability is subserved by different genes related to each trait (Pearce et al.,2017; Uzefovsky et al.,2014; Uzefovsky et al.,2015).

Further support is provided by neuroimaging studies showing that CE and EE differ in brain activation and structure (de Waal & Preston,2017; Shamay‐Tsoory et al.,2008; Uribe et al.,2019). CE depends on neocortical brain regions such as the ventromedial prefrontal cortex, whereas EE depends on subcortical regions such as the amygdala and the anterior cingulate cortex.

Of note, while most studies have focused on distinguishing the two traits, CE and EE‐related brain regions partially overlap, and regions specifically associated with each trait were suggested to interact when additional information is needed to engage with the feelings of others (Lamm et al.,2011; Preckel et al.,2018). For example, CE‐related brain regions interact with EE‐related brain regions, particularly during complex social situations in which additional processing is needed to jointly engage EE and CE (Lamm et al.,2011). As we constantly encounter complex social situations, these studies suggest that maintaining a balance between EE and CE is key for an adaptive and appropriate social response, leading to effective social communication.

Consistently, autistic individuals, which show marked difficulties in social communication, are usually reported as having intact EE but impaired CE (Baron‐Cohen,2013). Although this finding is supported by many empirical pieces of evidence (Gleichgerrcht et al.,2013; Mul et al.,2018; Rueda et al.,2015), other studies show mixed results (aan het Rot & Hogenelst,2014; Mazza et al.,2014; Scambler et al.,2007). For example, one study found that young autistic children displayed EE less frequently than non‐autistic children (Scambler et al.,2007). Another study used a common behavioral task to measure CE and classified autistic individuals into five subgroups, two of which did not differ in CE from non‐autistic individuals (Lombardo et al.,2016). These mixed findings suggest that the conceptualization of the social difficulties in autism as stemming from a deficit in CE, without the involvement of EE, is not quite accurate. Additionally, most previous studies of empathy in autism have examined the role of CE and EE independently, overlooking the possible interdependence between the two traits.

Trying to bridge this gap, we recently showed that empathic disequilibrium that is, the level of imbalance between CE and EE, predicted autistic traits in typical individuals, even after controlling for their total empathy (Shalev & Uzefovsky,2020). Specifically, we showed that autistic traits were elevated in a group of individuals with relatively higher EE than CE (EE‐dominance group) and found that EE‐dominance was related to social traits relevant to autism, such as alexithymia; but not to the non‐social traits, such as systemizing. These findings provide empirical evidence for the notion that an imbalance between CE and EE might contribute to some autistic symptoms (Smith,2009).

The current study aimed to examine the role of empathic disequilibrium in a large sample of clinically diagnosed autistic individuals to establish its relevance to autism. In our previous analysis, we used difference scores to compute empathic disequilibrium (Shalev & Uzefovsky,2020), yet such an approach suffers from some problems (see Edwards,1994, 1995 for a comprehensive review). Difference scores tend to be less reliable than each component separately, introducing possible bias to the results (Cronbach & Furby,1970). Moreover, by reducing the dimensionality of the two components, difference scores limit the interpretation of the results, making it harder to tell, in the current case, whether it was EE‐dominance or CE‐dominance that contributed to the prediction of autistic traits. To overcome these limitations, we now utilize polynomial regression with response surface analyses, providing a more nuanced and statistically valid methodology to examine the imbalance between CE and EE (Edwards & Parry,1993; Shanock et al.,2010). Polynomial regression with response surface analyses allows one to visualize and estimate the line of congruence, representing the degree to which similarity between variables is associated, both linearly and curvilinearly, with an outcome variable (see the blue line in Figure1); and the line of incongruence, which examines whether and how the discrepancy between two variables is related to an outcome (see the black line in Figure1). In this case, the line of incongruence represents empathic disequilibrium, and the line of congruence represents total empathy (the combination of EE and CE). Thus, we examine whether equilibrium and disequilibrium between EE and CE predict autism diagnosis and autistic traits (social and non‐social aspects).

Based on our previous findings (Shalev & Uzefovsky,2020), we hypothesized that both total empathy and empathic disequilibrium (with higher EE than CE) would predict autism and social traits related to autism. In contrast, empathic disequilibrium with higher CE than EE will predict non‐social traits related to autism (e.g., systemizing). Furthermore, as empathic disequilibrium also shows sex differences, we expected females to show a higher tendency towards EE‐dominance, relative to males, on average and across diagnostic groups.

METHODS

All participants signed informed consent before participation.

RESULTS

DISCUSSION

In line with our hypotheses, empathic disequilibrium and empathy independently predicted autism diagnosis and autistic traits in autistic and non‐autistic individuals. Specifically, lower total empathy and higher empathic disequilibrium towards EE‐dominance (higher emotional than cognitive empathy) predicted a greater likelihood of autism diagnosis, with additional non‐linear effects which relate to even higher/lower probability at the extremes of empathy and empathic disequilibrium. We also found that EE‐dominance is related to the social domain of autism, while CE‐dominance is related to the non‐social domain. In addition, females across diagnostic groups showed a greater tendency towards higher EE than CE.

This study provides empirical evidence that empathic disequilibrium is at least as informative as empathy for predicting autism diagnosis and is also valuable for predicting autistic traits in both autistic and non‐autistic populations. Empathic disequilibrium offers a new understanding of how autistic people might experience empathy that could solve some of the inconsistencies reported when EE and CE are examined separately (Mazza et al.,2014; Mul et al.,2018). Altogether, such conceptualization might better coincide with the inner experience of some autistic individuals reporting “excess of empathy” (Gillespie‐Lynch et al.,2017) and move beyond the still prevailing conceptualization that autism is associated with a lack of empathy, leading to stigmatization and a negative impact on the autistic community (Fletcher‐Watson & Bird,2020).

Empathic disequilibrium could advance the field by generating novel hypotheses. For example, we showed that, on average, autistic people tend to show empathic disequilibrium with a tendency towards EE‐dominance, but how would such an imbalance manifest? A person with empathic disequilibrium towards EE‐dominance might understand others' mental states (CE), but her/his ability to respond to these mental states (EE) will be relatively higher. Smith (2009) theoretically suggested that this state could cause overarousal, as the individual becomes overwhelmed with the other's emotions. The cognitive and behavioral characteristics of autistic individuals might constitute an adaptive response to overarousal.

The idea that empathy might be linked to overarousal in autism is also reflected by the non‐linear associations between empathy (both total empathy and empathic disequilibrium), autism diagnosis, and some autistic traits in our study. Some researchers suggest that extreme (high or low) levels of empathy can lead to overarousal and impair psychological functioning (Schipper & Petermann,2013; Tully et al.,2016). If this is the case in autism – where problems in emotion‐regulation are common (Cai et al.,2018; Mazefsky et al.,2013) ‐ emotional dysregulation may be driven by empathic disequilibrium or extreme levels of total empathy. While it is clear that empathy and emotion regulation are interrelated, this field is in its infancy and the links are currently unclear (Thompson et al.,2019). Further investigation into the mechanism hypothesized here between empathic disequilibrium and problems in emotion‐regulation could shed light on the role of emotion‐regulation in empathy, and the possible involvement of such a link in the manifestation of some autistic traits.

Our findings also suggest that not only is empathic disequilibrium towards EE‐dominance important (since it is associated with social autistic traits), but also empathic disequilibrium towards CE‐dominance, because it is associated with non‐social autistic traits. This was particularly strong in the non‐autistic population, fully replicating our previous results in a neurotypical population (Shalev & Uzefovsky,2020). Thus, while most autistic individuals lean towards EE‐dominance, CE‐dominance is also associated, albeit to a lesser extent, with an autism diagnosis. This highlights the possible involvement of CE‐dominance in autism as well. It is possible that both extremes of empathic disequilibrium are associated with autism through different pathways – EE‐dominance through difficulties in the social domain and CE‐dominance through the non‐social domain. This interpretation is consistent with a rich literature supporting deviation from homeostasis in either direction underlying the autism spectrum the autistic spectrum (e.g., Auerbach et al.,2011; Jeste & Geschwind,2014; Tatavarty et al.,2020; Villa et al.,2022). This suggests that the concept of empathic disequilibrium may help us focus on one of the sources of this manifest heterogeneity based on individuals' distinct empathic disequilibrium profiles.

The variability characterizing autism is also reflected in sex differences (Bedford et al.,2020). Studies suggest that autistic females tend to show different characteristics than autistic males, such as increased use of masking of their social difficulties (Hull et al.,2020). Together with the relatively limited research on autistic females, high rates of misdiagnosis have been suspected, stressing the need to better define this group (Kreiser & White,2014; Loomes et al.,2017). Previous research examining sex differences in empathy could not differentiate autistic males and females based on self‐reported empathy measured by the EQ (for a systematic review, see Kok et al.,2016). However, here we observed average sex differences in empathic disequilibrium, with autistic females displaying EE‐dominance more strongly than autistic males. This suggests that empathic disequilibrium might be of particular relevance to autistic females, providing a new lead into the emotional and cognitive characteristics of autistic females that should be further pursued.

Although substantial differences in empathic disequilibrium were found between autistic and non‐autistic individuals, our data suggest that empathic disequilibrium does not uniquely characterize autism and could be informative for the non‐autistic population as well, where it is associated with autistic traits. Therefore, empathic disequilibrium could provide new avenues of research that are not limited to the autistic population. For instance, empathic disequilibrium could be utilized to generate new hypotheses regarding the development of empathy. Throughout early development, EE remains relatively stable while CE steadily increases (Uzefovsky & Knafo‐Noam,2017). This might suggest that children show age‐typical EE‐dominant responses, and these diminish throughout early development until reaching balance in adulthood. Although our sample has a relatively large age range, it included only adults. Therefore, we were unable to examine earlier empathic disequilibrium development. Indeed, extensive changes in brain networks underlying empathic components and the connectivity between them occur during earlier periods of development until maturity in early adulthood (Decety,2010; Decety & Michalska,2010; Gogtay et al.,2004). Future research adopting a developmental approach in younger participants could clarify how and when some individuals come to experience empathic disequilibrium in adulthood while others do not.

Our study has several limitations. First, all measures used in our study are self‐report questionnaires. Although these measures are validated and correlate with other behavioral measures (Baron‐Cohen et al.,2001; Baron‐Cohen et al.,2003; Baron‐Cohen & Wheelwright,2004; Lawrence et al.,2004), they primarily reflect the participants' perception of their own functioning and ability. However, while observational methods offer rich information, empathy is largely an internally experiential process that cannot be inferred from behavior alone (Hoffman,2001), suggesting that self‐report measures are valuable tools for understanding empathy.

Second, the use of questionnaires filled online further limits our conclusions. Participating in such a study requires interest in research, the ability to sign up for it, and the ability to fill it out, suggesting that the sample used in our study consists mainly of autistic individuals with average or above‐average intelligence, likely excluding individuals with intellectual disabilities. As such, our sample does not represent the entire autistic spectrum, where intellectual disability is common and reflects part of the heterogeneity characterizing autism (Lecavalier et al.,2011). Future research examining empathic disequilibrium using behavioral measures of empathy could overcome these limitations and benefit from extending our findings to the entire autistic spectrum. We see the current work as a proof‐of‐concept for the importance of empathic disequilibrium, and this can serve as the basis for developing and validating a behavioral measure for empathic disequilibrium measurement across the autistic spectrum.

Furthermore, the non‐autistic group also included family members of diagnosed individuals, suggesting that this group might be representative of the broad autism phenotype, i.e., people who carry genetic liability for autism and/or display milder phenotypic features (Hurst et al.,2007; Piven et al.,1997). Yet even in this population as a comparison group, we see significant differences as compared to the autistic group.

This study focuses on empathic disequilibrium as an informative index for the diagnosis of autism and for predicting autistic traits in both autistic and non‐autistic populations. By offering a novel way to examine the role of empathy in autism, empathic disequilibrium may better reflect the experience of some autistic individuals. Further research is needed to translate these insights into tools for prognosis, diagnosis, and intervention in autism.

CONFLICT OF INTEREST

All of the funding organizations had no role in any part of the study including the design and conduct of the study, collection, analysis, interpretation of data, or the writing of the manuscript. All authors declare no conflicts of interest.

ETHICS STATEMENT

Ethical approval for the research database was obtained from the Psychology Research Ethics Committee, University of Cambridge, United Kingdoms.

Supporting information

ACKNOWLEDGMENTS

Florina Uzefovsky was supported by the National Institute for Psychobiology in Israel (NIPI), and by the Israel Science Foundation (Grant No. 449/14). Ido Shalev was supported by a Negev scholarship granted by Ben‐Gurion University of the Negev. Simon Baron‐Cohen received funding from the Wellcome Trust 214322\Z\18\Z. In addition, Simon Baron‐Cohen received funding from Innovative Medicines Initiative 2 Joint Undertaking (JU) under grant agreement No 777394. The JU receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. Simon Baron‐Cohen also received funding from the Autism Research Trust, the Templeton World Charitable Fund, the MRC, SFARI, and the NIHR Cambridge Biomedical Research Centre. The research was supported by the National Institute for Health Research (NIHR) Collaboration for Leadership in Applied Health Research and Care East of England at Cambridgeshire and Peterborough NHS Foundation Trust. The views expressed are those of the author(s) and not necessarily those of the NHS, NIHR or Department of Health and Social Care.

Notes

Shalev, I., Warrier, V., Greenberg, D. M., Smith, P., Allison, C., Baron‐Cohen, S., Eran, A., & Uzefovsky, F. (2022). Reexamining empathy in autism: Empathic disequilibrium as a novel predictor of autism diagnosis and autistic traits. Autism Research, 15(10), 1917–1928. 10.1002/aur.2794 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

Funding information Autism Research Trust; Innovative Medicines Initiative, Grant/Award Number: 777394; Israel Science Foundation, Grant/Award Number: 449/14; Kreitman School of Advanced Graduate Studies, Ben‐Gurion University of the Negev; Medical Research Council; National Institute for Psychobiology in Israel, Hebrew University of Jerusalem; Peterborough NHS Foundation Trust; Simons Foundation Autism Research Initiative; Templeton World Charitable Fund; Wellcome Trust, Grant/Award Number: 214322\Z\18\Z; Department of Health; Health Research; National Institute for Health Research; Biomedical Research Centre; AUTISM SPEAKS; Horizon 2020; European Union; Ben‐Gurion University of the Negev

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

REFERENCES