Autistic Empathy Toward Autistic Others
Individuals with autism spectrum disorder (ASD) are thought to lack self-awareness and to experience difficulty empathizing with others. Although these deficits have been demonstrated in previous studies, most of the target stimuli were constructed for typically developing (TD) individuals. We employed judgment tasks capable of indexing self-relevant processing in individuals with and without ASD. Fourteen Japanese men and 1 Japanese women with high-functioning ASD (17–41 years of age) and 13 Japanese men and 2 TD Japanese women (22–40 years of age), all of whom were matched for age and full and verbal intelligence quotient scores with the ASD participants, were enrolled in this study. The results demonstrated that the ventromedial prefrontal cortex was significantly activated in individuals with ASD in response to autistic characters and in TD individuals in response to non-autistic characters. Although the frontal–posterior network between the ventromedial prefrontal cortex and superior temporal gyrus participated in the processing of non-autistic characters in TD individuals, an alternative network was involved when individuals with ASD processed autistic characters. This suggests an atypical form of empathy in individuals with ASD toward others with ASD.
As suggested by the term 'autism', which comes from the Greek word autós, meaning self, a lack of self-awareness is a central element of autism spectrum disorder (ASD) (Toichi et al., 2002; Lombardo et al., 2010). Deficits in self-related processing lead to difficulties in empathizing with others (Lombardo et al., 2007). Individuals with ASD also show deficits in reciprocal social interactions and impairment in verbal communication, such as difficulties in understanding humor, irony and sarcasm (Frith, 2003). These pragmatic language impairments are thought to be based on deficits in theory of mind, the ability to attribute mental states to oneself and to others. This ability to make inferences about what other people think allows one to predict their behaviors (Baron-Cohen et al., 1985). During the process involved in making inferences, the theory of mind network, including the medial prefrontal cortex, precuneus (and posterior cingulate cortex) and temporoparietal junction (and adjunct superior temporal sulcus), is recruited when individuals reflect on themselves and others (Amodio and Frith, 2006; Frith and Frith, 2006; Mitchell et al., 2006a,b; Saxe et al., 2006; Lombardo et al., 2010). Several brain imaging studies have investigated the neural basis of theory of mind in TD individuals (Fletcher et al., 1995; Baron-Cohen et al., 1999; Castelli et al., 2000; Gallagher et al., 2000, 2002; Vogeley et al., 2001; Ferstl and von Cramon, 2002). The theory of mind network is altered in ASD (Mason et al., 2008; Mizuno et al., 2011; Morita et al., 2012).
Observations in ASD groups lacking theory of mind and/or empathy as well as recent neuroimaging research have provided empirical evidence of a neural basis for theory of mind and empathy (Völlm et al., 2006; Bird et al., 2010). Impairment in theory of mind has been implicated in neurodevelopmental disorders in ASD (Lombardo et al., 2007). Additionally, previous studies on brain connectivity have demonstrated that the degree of synchronization in activation (i.e. functional connectivity) between frontal and posterior brain regions is lower in ASD. The first report of this nature was in the context of a language comprehension task (Just et al., 2004); undersynchronization of activation during cognitive tasks has been reported between the frontal lobe and more posterior regions in several other paradigms (Just et al., 2004, 2012; Kana et al., 2006, 2009).
Although deficits in ASD have been demonstrated in previous studies, most of the target stimuli used in those studies were constructed for typically developing (TD) individuals. However, it may be difficult for individuals with ASD to understand TD individuals, just as it is difficult for TD individuals to understand those with ASD. Concerning the similarity between self and other brain regions, ventral parts of the medial prefrontal cortex (mPFC) respond both during self-referential processing (Kelley et al., 2002; Northoff et al., 2006) and during mental state inferences concerned with others (Gallagher et al., 2000, 2002; Frith and Frith, 2006). The neural substrates underlying self-referential thought and theory of mind are characterized by overlap (Mitchell et al., 2005, 2006b; Jenkins et al., 2008; Tamir and Mitchell, 2010).
Previous studies demonstrated a lack of preferential responsiveness to self-information in the ventromedial prefrontal cortex (vmPFC) in individuals with ASD (Lombardo et al., 2010; Pfeifer et al., 2013). Compared with those with ASD, TD individuals recruited the vmPFC to a significantly greater extent for self vs. other in the reflective mentalizing task and in tasks pertaining to physical self-judgments and the British Queen. Previous behavioral studies have demonstrated that individuals with ASD do not benefit from self-referential elaboration (Toichi et al., 2002; Lombardo et al., 2007) and display a lack of 'neural self-reference effect' in the vmPFC (Lombardo et al., 2010).
When readers and characters are matched in personality, TD readers empathize with story characters similar to themselves (Komeda et al., 2013b). If this were also the case for individuals with ASD, these individuals may show empathy, a process in which one identifies with similar others. Additionally, the self-related brain network of individuals with ASD may participate in interactions with targets who have autistic traits. We used self- and other judgment tasks to test these hypotheses (Figure 1). Participants read sentences and responded to questions about them using two buttons (Yes and No). On the basis of the items in the Social Responsiveness Scale (SRS; Constantino and Todd, 2005; Kamio et al., 2009, 2013), each sentence described the behavior of a target character with traits identified as autistic or non-autistic. For example, self-judgments and other judgments about autistic and non-autistic characters involved participants' reading a description about a character (e.g. 'I would rather be alone than with others' and 'Yuya would rather be with others than be alone', respectively) and evaluating their identification with this description (i.e. 'Do you agree with the sentence?' and 'Do you think you are similar to him?'). Sex was matched between participant and character.
(Enlarge Image)
Figure 1.
We employed a block design for the experiment. Schematic depiction of stimuli and task design of each block in the fMRI study. First, a fixation crosshair was presented, followed by the experimental stimuli, which were displayed for 5.75 s. The top line in each stimulus-containing rectangle presented a question ('Do you agree with the sentence?' for a self-task and 'Do you think you are similar to him/her for an other task'), and the bottom line described a response with or without autistic traits.
We predicted that similarities between perceivers and targets would facilitate empathy, leading to selective responses toward targets similar to themselves. This prediction is known as the similarity hypothesis (Komeda et al., 2013a,b). Recent studies on TD adults have demonstrated that similarities between readers and characters play a critical role in cognitive tasks such as story comprehension and memory. For example, personality is an important contributor to similarities between readers and characters (Komeda et al., 2009, 2013b). Indeed, it is easier for highly extraverted than for less extraverted participants to understand stories about a highly extraverted story character (Komeda et al., 2009). Additionally, highly extraverted readers judge the behavioral outcomes of highly extraverted fictional characters more rapidly than do less extraverted readers, and highly neurotic readers judge the outcomes of highly neurotic characters more rapidly than do less neurotic readers (Komeda et al., 2013b).
Individuals with ASD provide specific responses to autistic fictional characters (Komeda et al., 2013a). For example, in the case of episodes about ASD characters, individuals with ASD more effectively retrieved consistent outcomes than inconsistent outcomes, and TD individuals retrieved stories with TD characters more effectively than stories with autistic characters. Thus, similarity between reader and fictional character had different effects on the memory retrieval of individuals with and without ASD.
In this study, we used functional magnetic resonance imaging (fMRI) to investigate whether activation of the vmPFC, known to be involved in self-related information processing (Lombardo et al., 2007; Tamir and Mitchell, 2010; Pfeifer et al., 2013) and empathy (Shamay-Tsoory et al., 2009; Schulte-Rüther et al., 2011; Shamay-Tsoory, 2011), was observed when participants made judgments about characters similar to themselves. We also examined whether seed-to-voxel functional connectivity differed among groups.
Abstract and Introduction
Abstract
Individuals with autism spectrum disorder (ASD) are thought to lack self-awareness and to experience difficulty empathizing with others. Although these deficits have been demonstrated in previous studies, most of the target stimuli were constructed for typically developing (TD) individuals. We employed judgment tasks capable of indexing self-relevant processing in individuals with and without ASD. Fourteen Japanese men and 1 Japanese women with high-functioning ASD (17–41 years of age) and 13 Japanese men and 2 TD Japanese women (22–40 years of age), all of whom were matched for age and full and verbal intelligence quotient scores with the ASD participants, were enrolled in this study. The results demonstrated that the ventromedial prefrontal cortex was significantly activated in individuals with ASD in response to autistic characters and in TD individuals in response to non-autistic characters. Although the frontal–posterior network between the ventromedial prefrontal cortex and superior temporal gyrus participated in the processing of non-autistic characters in TD individuals, an alternative network was involved when individuals with ASD processed autistic characters. This suggests an atypical form of empathy in individuals with ASD toward others with ASD.
Introduction
As suggested by the term 'autism', which comes from the Greek word autós, meaning self, a lack of self-awareness is a central element of autism spectrum disorder (ASD) (Toichi et al., 2002; Lombardo et al., 2010). Deficits in self-related processing lead to difficulties in empathizing with others (Lombardo et al., 2007). Individuals with ASD also show deficits in reciprocal social interactions and impairment in verbal communication, such as difficulties in understanding humor, irony and sarcasm (Frith, 2003). These pragmatic language impairments are thought to be based on deficits in theory of mind, the ability to attribute mental states to oneself and to others. This ability to make inferences about what other people think allows one to predict their behaviors (Baron-Cohen et al., 1985). During the process involved in making inferences, the theory of mind network, including the medial prefrontal cortex, precuneus (and posterior cingulate cortex) and temporoparietal junction (and adjunct superior temporal sulcus), is recruited when individuals reflect on themselves and others (Amodio and Frith, 2006; Frith and Frith, 2006; Mitchell et al., 2006a,b; Saxe et al., 2006; Lombardo et al., 2010). Several brain imaging studies have investigated the neural basis of theory of mind in TD individuals (Fletcher et al., 1995; Baron-Cohen et al., 1999; Castelli et al., 2000; Gallagher et al., 2000, 2002; Vogeley et al., 2001; Ferstl and von Cramon, 2002). The theory of mind network is altered in ASD (Mason et al., 2008; Mizuno et al., 2011; Morita et al., 2012).
Observations in ASD groups lacking theory of mind and/or empathy as well as recent neuroimaging research have provided empirical evidence of a neural basis for theory of mind and empathy (Völlm et al., 2006; Bird et al., 2010). Impairment in theory of mind has been implicated in neurodevelopmental disorders in ASD (Lombardo et al., 2007). Additionally, previous studies on brain connectivity have demonstrated that the degree of synchronization in activation (i.e. functional connectivity) between frontal and posterior brain regions is lower in ASD. The first report of this nature was in the context of a language comprehension task (Just et al., 2004); undersynchronization of activation during cognitive tasks has been reported between the frontal lobe and more posterior regions in several other paradigms (Just et al., 2004, 2012; Kana et al., 2006, 2009).
Although deficits in ASD have been demonstrated in previous studies, most of the target stimuli used in those studies were constructed for typically developing (TD) individuals. However, it may be difficult for individuals with ASD to understand TD individuals, just as it is difficult for TD individuals to understand those with ASD. Concerning the similarity between self and other brain regions, ventral parts of the medial prefrontal cortex (mPFC) respond both during self-referential processing (Kelley et al., 2002; Northoff et al., 2006) and during mental state inferences concerned with others (Gallagher et al., 2000, 2002; Frith and Frith, 2006). The neural substrates underlying self-referential thought and theory of mind are characterized by overlap (Mitchell et al., 2005, 2006b; Jenkins et al., 2008; Tamir and Mitchell, 2010).
Previous studies demonstrated a lack of preferential responsiveness to self-information in the ventromedial prefrontal cortex (vmPFC) in individuals with ASD (Lombardo et al., 2010; Pfeifer et al., 2013). Compared with those with ASD, TD individuals recruited the vmPFC to a significantly greater extent for self vs. other in the reflective mentalizing task and in tasks pertaining to physical self-judgments and the British Queen. Previous behavioral studies have demonstrated that individuals with ASD do not benefit from self-referential elaboration (Toichi et al., 2002; Lombardo et al., 2007) and display a lack of 'neural self-reference effect' in the vmPFC (Lombardo et al., 2010).
When readers and characters are matched in personality, TD readers empathize with story characters similar to themselves (Komeda et al., 2013b). If this were also the case for individuals with ASD, these individuals may show empathy, a process in which one identifies with similar others. Additionally, the self-related brain network of individuals with ASD may participate in interactions with targets who have autistic traits. We used self- and other judgment tasks to test these hypotheses (Figure 1). Participants read sentences and responded to questions about them using two buttons (Yes and No). On the basis of the items in the Social Responsiveness Scale (SRS; Constantino and Todd, 2005; Kamio et al., 2009, 2013), each sentence described the behavior of a target character with traits identified as autistic or non-autistic. For example, self-judgments and other judgments about autistic and non-autistic characters involved participants' reading a description about a character (e.g. 'I would rather be alone than with others' and 'Yuya would rather be with others than be alone', respectively) and evaluating their identification with this description (i.e. 'Do you agree with the sentence?' and 'Do you think you are similar to him?'). Sex was matched between participant and character.
(Enlarge Image)
Figure 1.
We employed a block design for the experiment. Schematic depiction of stimuli and task design of each block in the fMRI study. First, a fixation crosshair was presented, followed by the experimental stimuli, which were displayed for 5.75 s. The top line in each stimulus-containing rectangle presented a question ('Do you agree with the sentence?' for a self-task and 'Do you think you are similar to him/her for an other task'), and the bottom line described a response with or without autistic traits.
We predicted that similarities between perceivers and targets would facilitate empathy, leading to selective responses toward targets similar to themselves. This prediction is known as the similarity hypothesis (Komeda et al., 2013a,b). Recent studies on TD adults have demonstrated that similarities between readers and characters play a critical role in cognitive tasks such as story comprehension and memory. For example, personality is an important contributor to similarities between readers and characters (Komeda et al., 2009, 2013b). Indeed, it is easier for highly extraverted than for less extraverted participants to understand stories about a highly extraverted story character (Komeda et al., 2009). Additionally, highly extraverted readers judge the behavioral outcomes of highly extraverted fictional characters more rapidly than do less extraverted readers, and highly neurotic readers judge the outcomes of highly neurotic characters more rapidly than do less neurotic readers (Komeda et al., 2013b).
Individuals with ASD provide specific responses to autistic fictional characters (Komeda et al., 2013a). For example, in the case of episodes about ASD characters, individuals with ASD more effectively retrieved consistent outcomes than inconsistent outcomes, and TD individuals retrieved stories with TD characters more effectively than stories with autistic characters. Thus, similarity between reader and fictional character had different effects on the memory retrieval of individuals with and without ASD.
In this study, we used functional magnetic resonance imaging (fMRI) to investigate whether activation of the vmPFC, known to be involved in self-related information processing (Lombardo et al., 2007; Tamir and Mitchell, 2010; Pfeifer et al., 2013) and empathy (Shamay-Tsoory et al., 2009; Schulte-Rüther et al., 2011; Shamay-Tsoory, 2011), was observed when participants made judgments about characters similar to themselves. We also examined whether seed-to-voxel functional connectivity differed among groups.
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