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Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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26 mai 2013
Front Hum Neurosci.
2013
Structural basis of empathy
and the domain general region
in the anterior insular cortex
 
Mutschler I, Reinbold C, Wankerl J, Seifritz E, Ball T.

Chat-logomini

 
Abstract
 
Empathy is key for healthy social functioning and individual differences in empathy have strong implications for manifold domains of social behavior. Empathy comprises of emotional and cognitive components and may also be closely linked to sensorimotor processes, which go along with the motivation and behavior to respond compassionately to another person's feelings. There is growing evidence for local plastic change in the structure of the healthy adult human brain in response to environmental demands or intrinsic factors. Here we have investigated changes in brain structure resulting from or predisposing to empathy. Structural MRI data of 101 healthy adult females was analyzed. Empathy in fictitious as well as real-life situations was assessed using a validated self-evaluation measure. Furthermore, empathy-related structural effects were also put into the context of a functional map of the anterior insular cortex (AIC) determined by activation likelihood estimate (ALE) meta-analysis of previous functional imaging studies. We found that gray matter (GM) density in the left dorsal AIC correlates with empathy and that this area overlaps with the domain general region (DGR) of the anterior insula that is situated in-between functional systems involved in emotion-cognition, pain, and motor tasks as determined by our meta-analysis. Thus, we propose that this insular region where we find structural differences depending on individual empathy may play a crucial role in modulating the efficiency of neural integration underlying emotional, cognitive, and sensorimotor information which is essential for global empathy.
insula
Introduction
 
Empathy has strong implications for manifold domains of social behavior and it may constitute an integral part of emotional intelligence (Goleman, 1998). In the psychological literature, empathy has been defined as the ability to feel what another person is feeling (emotional component), and knowing what a person is feeling (cognitive component), i.e., to achieve a cognitive understanding of other feelings (Eisenberg and Miller, 1987; Decety and Jackson, 2004). Empathy may also include sensorimotor processes, which go along with the motivation and behavior to respond compassionately to another person's feelings (Preston, 2007; Zaki and Ochsner, 2012). It has been shown that empathetic ability, however, is not always going along with prosocial behavior (Eisenberg and Miller, 1987).
 
The cognitive component of empathy may be closely linked to "theory of mind," that is the meta-cognitive ability to represent mental states such as beliefs, intentions, and desires of other people (Premack and Woodruf, 1978). According to Dymond, an empathic person can imaginatively take the role of another and can understand and predict that person's thoughts, feelings, and actions (Dymond, 1949). Together, these definitions suggest that the human ability of empathy is more than a pure emotional process but also includes cognitive aspects such as perspective taking and may also involve the sensorimotor system for responding appropriately and compassionately to another person's feelings. There is growing appreciation that there are stable differences between individuals in the level of empathy which has a high impact on social behavior (Zaki and Ochsner, 2012) and that these differences can be reliably measured (Miller and Eisenberg, 1988; Marangoni et al., 1995; Singer et al., 2004).
 
Recent studies have shown that there is capacity for local plastic change in the structure of the healthy adult human brain in response to environmental demands or intrinsic factors (Johansen-Berg, 2012). There is increasing interest in investigating the neuroanatomical basis underlying individual differences in human behavior and cognition (Kanai and Rees, 2011), including empathy (Banissy et al., 2012). However, the structural basis of empathy in particular in the insular cortex has remained unclear. Accumulating evidence indicates a crucial role of the insular cortex in empathy: in particular the anterior insular cortex (AIC)a brain region which is situated in the depth of the Sylvian fissure and anatomically highly interconnected to many other cortical regions (Nieuwenhuys, 2012) is part of the functional neural network that plays an essential role in mediating social-emotional processing (Mutschler et al., 2009, 2012) including empathy (Singer et al., 2004; Seeley et al., 2012).
insula insula
Discussion
 
Our results indicate regionally specific structural differences in the left dorsal AIC related to individual empathy scores in healthy individuals. GM density correlated in a confined region of the left dorsal AIC with empathy in healthy females. The insular region where we find structural differences overlaps with the peaks from a previous functional study correlating empathy-related responses fMRI with individual empathy scores (Singer et al., 2004), Figure 2B. This precise spatial correspondence strongly supports our VBM findings. Studies show that individuals with specialized abilities have markedly developed brain structures in specific regions related to their expertise (Kanai and Rees, 2011). For instance, an investigation by Maguire et al. on London taxi drivers found that GM measures derived from T1-weighted structural MRI are sensitive to experience. The authors showed that taxi drivers, with their knowledge of London's complex street plan, had enlarged posterior hippocampi in comparison to control subjects (Maguire et al., 2000). More recently, a longitudinal study demonstrates that learning to juggle increases GM density in occipito-parietal cortical areas in the adult brain involved in reaching and grasping (Scholz et al., 2009).
 
The results reveal that our morphometrically identified area in the dorsal AIC related to individual differences in empathy overlaps the DGR. A first indication toward a DGR was provided by Dosenbach et al. who conjointly analyzed mixed design fMRI experiments using 10 different tasks (Dosenbach et al., 2006). They found, among others, the bilateral anterior insula/frontal operculum region to show reliable start-cue and sustained activations across all or nearly all tasks. This generalized type of activation was found in the dorsal part of the AIC (black dot in Figure 2). The idea of a DGR was extended by Craig in his review on awareness and the AIC (Craig, 2009).
 
The author observed that, in imaging studies, the AIC is reported to be activated in an astonishing number of studies from a broad range of topics including all types of subjective feelings, attention, cognitive choices, intentions, music, time perception, awareness of sensations, and movements, of visual and auditory percepts, of the trustworthiness of other individuals and concluded that "No other region of the brain is activated in all of these tasks." In a subsequent meta-analysis of a wide range of functional imaging studies, the same region of the AIC that showed task-set-related responses in the study by Dosenbach et al. was also reliably activated by a wide range of auditory and language tasks as well as during social norm violation (Mutschler et al., 2009). Importantly, this study was restricted to studies which reported clear insular responses, i.e., ambiguous effects such as "insula/frontal operculum" were excluded, giving strong additional support for the existence of a domain-general region in the AIC. The idea of a DGR that is activated across nearly all kinds of tasks as well as Craig's observation that no other brain region shows such generalized responses was later also confirmed in a meta-analysis (Kurth et al., 2010).
 
However, little is known regarding the exact location and the functional meaning of the DGR in the dorsal AIC. There is good evidence that the DGR is found in the dorsal anterior insula as indicated in Figure 2A. Importantly, compared to a previous interpretation (Brown et al., 2011) our ALE analysis shows that movement-related responses do not (or only to a very small degree) overlap with the domain-general area. The position of the main region with reproducible movement-related responses is located just posterior to the domain-general region (blue area in Figure 2). This movement-related area closely co-localized with insular peaks related to the sense of agency of hand movements (Mutschler et al., 2009). What is the functional meaning of the DGRin particular for empathy? Several overarching functions have been proposed such as task-set processing (Dosenbach et al., 2006) and a role in awareness (Craig, 2009). Importantly, our findingsthat the morphometrically identified area in the dorsal AIC related to individual differences in empathy overlaps the DGRsupport the notion that its underlying neuronal substrate may be involved in integrating socio-emotional information during empathy.
 
We find that emotion-related responses in healthy subjects were preferentially located in the dorsal AIC. This region was distinct from the insular region associated with peripheral physiological changes resulting from emotional experiences and found that this activity was represented in the ventral AIC that was also the most likely site of insular co-activation with the amygdala (Mutschler et al., 2009). In the current study, insula-coordinates associated with emotion-related peripheral physiological changes were excluded. Therefore, our findings suggest that distinct functional insula regions may be involved in different aspects of emotional processing, whereby peripheral physiological correlates of emotional processing are mapped to the ventral anterior regions, while emotion-cognitive processes are mapped to a more dorsal-anterior region. More specifically, we assume that the dorsal anterior insula might play a pivotal role in integrating sensory stimuli with its salience, possibly via connections to the cingulate cortex. This interpretation is supported by the fact that in our study-sample subjects evaluated the emotional content of the presented stimuli and in direct agreement with recent findings showing that the dorsal anterior insula is more consistently involved in human cognition than ventral anterior and posterior networks (Chang et al., 2013), and the observed functional connectivity between the dorsal anterior insula and the dorsal anterior cingulate cortex, which that plays a crucial role in cognitive decision-making (Deen et al., 2011). Pain-related maximal ALE were found in the posterior insula and in the dorsal AIC. Both, emotion and pain related ALE findings are discussed in more detail elsewhere (Mutschler et al., 2012) because the aim of this meta-analysis was to relate them to studies on empathy.
 
Recent neuroimaging studies show that the anterior insula and the anterior cingulate cortex are engaged during both, the experience and observation of pain (Singer et al., 2004; Lamm et al., 2011). It has been suggested that neural responses involved in both conditions might reflect a neuronal substrate which is related to the affective but not sensory aspect of pain (Singer et al., 2004). Together, our present ALE-findings support this notion and suggest that the posterior insula is involved in processing sensory aspect of pain, whereas the dorsal anterior insula is involved in emotion. In summary, we argue that the dorsal AIC plays a pivotal role in empathy (similarly as during emotion processing and pain) by integrating sensory stimuli with its salience, possibly via connections to the cingulate cortex. This assumption is also supported by the fact that ALE-findings related to emotion and empathy for pain and also the DGRwhich has been associated with cognitionoverlap in the dorsal anterior insula, suggesting that these functions share a common neural substrate (Dosenbach et al., 2006). As mentioned above we assume that the overall role of the morphometrically identified area in the dorsal AIC related to individual differences in empathy which overlaps the DGR might be involved in integrating information which is relevant for socio-emotional and cognitive processing. Thus, we assume that empathy is not (only) related to a specific "socio-emotional" interaction area, but to a superordinate "domain-general" area, in line with concepts of empathy that include not only social and emotional, but also cognitive aspects (Eisenberg and Miller, 1987; Decety and Jackson, 2004). Whether our findings in the dorsal AIC have also a relation to the "von Economo neurons" [VENs, (Von Economo, 1926)] remains to be determined. VENs have been hypothesized to play are role in social-emotional processing including empathy (Evrard et al., 2012; Seeley et al., 2012).
 
In the following paragraph potential limitations of this study are discussed and suggestions are made for future research. Similarly to previous imaging studies (e.g., Singer et al., 2004) we have investigated correlates of overall empathy in our study by using a widely applied and validated self-evaluation measure (Leibetseder et al., 2001, 2007). There is a potential concern about the influence of the social desirability biaswhich refers to the tendency of subjects to answer self report items in a self-favoring manneron the validity of questionnaire-based research (Edwards, 1957). It is discussed whether social desirability scales may be used to detect, minimize, and correct for social desirability bias in order to improve the validity of questionnaire-based research (e.g., Uziel, 2010). In a future study it would be interesting to measure empathy experimentallye.g., by investigating the impact of compassion-based meditation on empathy (Mascaro et al., 2013)and to relate functional activity to GM properties.
 
In this study, brain structure changes resulting from or predisposing to empathy have been investigated in a large sample of females because of increasing evidence for sex differences in empathy. Females score on average higher than males on self-report measures of empathy (Hoffman, 1977; Baron-Cohen and Wheelwright, 2004). Singer et al. observed in an fMRI study on empathy for pain that in males but not females empathetic reactions were absent for persons who were perceived as behaving unfairly (Singer et al., 2006). Recently, Van Honk et al. (2011) showed that the administration of the androgen hormone testosteronewhich represents the largest hormonal difference between the sexesimpaired cognitive empathy in healthy females. As mentioned, the insular region where we find structural differences exactly overlaps with the peaks from a previous functional study correlating empathy-related responses fMRI with individual empathy scores (Singer et al., 2004). Notably, in this study also only females were investigated. A recent study found in a sample with mixed gender individual differences in trait empathy dimensions correlating with morphological differences in several brain areas including the anterior cingulated cortex and the right dorsolateral prefrontal cortex (Banissy et al., 2012). More specifically, based on an analysis with ROIs around peaks from previous functional studies on empathy, Banissy et al. report structural changes in the ventral-most part of the insular cortex, several centimeters apart from the area characterized in the present study.
 
Interpretational difficulties however arise because (1) the peak at MNI coordinates -39, 9, -21 as reported by Banissy et al. (that was used to define the ventral insular ROI) is pain-related and not empathy-related as was assumed by the authors (see Appendix to Singer et al., 2004) and (2) a second, empathic concern-related peak reported to be in the insular region by Banissy et al. at MNI coordinates -48, 6, 18 is according to the probabilistic assignment obtained from the SPM Anatomy Toolbox (Eickhoff et al., 2005) located in Brodmann Area 44. In this study, structural changes specific to males or females were however not addressed and only changes that were consistent across the whole (mixed) sample were reported which may possibly explain the different results of their and our study. Alternatively, the different results between both studies may also be explained by the fact that in our study the focus was on global empathy whereas in the study by Banissy et al. on the relationship between components of empathy (empathic concern, personal distress, perspective taking, and fantasizing) and brain structure using a different measure. Because empathy crucially requires high-level integration of emotional, cognitive, and social components as well as of behavioral control the goal of our study was not to investigate different components of empathy but to explore the neural substrate that may underlay its neural integration. Our interpretationthat the dorsal AIC where we find structural differences depending on individual empathy might play a crucial role in modulating the efficiency of neural integration underlying emotional, cognitive, and sensorimotor information which is essential for global empathy is in agreement with previous studies reporting that reduced GM volume in the AIC was associated with a lack of empathy in neuropsychiatric disorders such as in conduct disorder (Sterzer et al., 2007) and in psychopathy (de Oliveira-Souza et al., 2008). Further, as mentioned above, a recent study in combat veterans with traumatic brain injury shows that lesions in several brain regions, particularly in the insula, was associated with deficits in empathy (Driscoll et al., 2012). In future research based on larger samples it would be interesting to investigate the role of empathy subscales such as cognitive and emotional components (Leibetseder et al., 2007), and their relation to functional and structural data. The emotional component of empathy has been for instance closely linked to activation in the inferior frontal gyrus (Shamay-Tsoory et al., 2009; Banissy et al., 2012).
 
Finally, longitudinal studies are needed to clarify whether the empathy-related structural effects in the dorsal AIC that we find are due to a pre-existing brain characteristic or to empathy-experience, or whether it indicates both.
 
In addition, all neuroimaging studies entering our meta-analysis reported that only healthy individuals free of any neurological and psychiatric disorders were investigated. However, for future meta-analyses it would be important that neuroimaging studies specify more clearly the procedure regarding how they assessed and excluded individuals with neurological and psychiatric disorders [e.g., whether a structured clinical interview for Diagnostic and Statistical Manual IV (DSM-IV) axis I and axis II personality disorders was used]. Furthermore, it is also important to note that our meta-analysis on empathy included females and males. An interesting topic for future meta-analyses would be to examine whether there are functional differences between male and female samples with respect to empathy. Finally, future meta-analyses should also investigate whether the dorsal AIC is rather involved in empathy for pain (Singer et al., 2004) and social rejection (Eisenberger et al., 2003) than in empathy for positive emotions and if yes why this could be the case. Only few brain imaging studies to date have examined empathy for positive emotions (Jabbi et al., 2007; Mobbs et al., 2009; Morelli et al., 2012), therefore ALE meta-analysis could not be performed. If the dorsal AIC is related to empathy and is essential for high-level integration, it should be activated during empathy for all types of emotions. However, the few studies on empathy for positive emotions suggest that the dorsal AIC might not be involved (Mobbs et al., 2009; Morelli et al., 2012), but a meta-analytic analysis based on a large sample of studies would be required to resolve this issue. In future it would be also important to meta-analytically examine studies on empathy for negative emotions which show insula activation, such as empathy for disgust (Wicker et al., 2003), embarrassment (Krach et al., 2011), social rejection (Masten et al., 2011), and anxiety (Morelli et al., 2012), as well as studies on functional components of empathy.
 
In summary, the dorsal AIC where we find structural differences depending on individual empathy may be key in modulating the efficiency of neural integration underlying emotional, cognitive, and sensorimotor information which is essential for empathy. Furthermore, our results support a functional subdivision of the human insula in functionally distinct regions. These include the ventral anterior insula which is involved in mapping peripheral physiological information during emotional experiences and the dorsal AIC which plays a crucial role in integrating sensory stimuli with salience possibly via connections to the cingulate cortex. The dorsal anterior insula constitutes an auditory and language area and the mid anterior insula plays a pivotal role in sensorimotor processing. Finally, the posterior insula may be involved in processing sensory aspects of nociceptive information and the dorsal AIC may have an integrative role during emotional-cognitive evaluation of a noxious stimuli and the associated sensorimotor response. Together, these findings provide new important insights into the functional organization of the human insular cortex in healthy individuals, and the functional map may be helpful for understanding dysfunction in conditions affecting empathy such as borderline personality disorder with co-morbid posttraumatic stress disorder, autistic spectrum disorders, psychopathy/antisocial personality disorder, conduct disorder, and schizophrenia.