Geoffrey Bird

Empathic brain responses in insula are modulated by levels of alexithymia but not autism

Difficulties in social cognition are well recognized in individuals with autism spectrum conditions (henceforth ‘autism’). Here we focus on one crucial aspect of social cognition: the ability to empathize with the feelings of another. In contrast to theory of mind, a capacity that has often been observed to be impaired in individuals with autism, much less is known about the capacity of individuals with autism for affect sharing. Based on previous data suggesting that empathy deficits in autism are a function of interoceptive deficits related to alexithymia, we aimed to investigate empathic brain responses in autistic and control participants with high and low degrees of alexithymia. Using functional magnetic resonance imaging, we measured empathic brain responses with an ‘empathy for pain’ paradigm assessing empathic brain responses in a real-life social setting that does not rely on attention to, or recognition of, facial affect cues. Confirming previous findings, empathic brain responses to the suffering of others were associated with increased activation in left anterior insula and the strength of this signal was predictive of the degree of alexithymia in both autistic and control groups but did not vary as a function of group. Importantly, there was no difference in the degree of empathy between autistic and control groups after accounting for alexithymia. These findings suggest that empathy deficits observed in autism may be due to the large comorbidity between alexithymic traits and autism, rather than representing a necessary feature of the social impairments in autism.

Levels of emotional awareness and autism: An fMRI study

Abstract Autism is associated with an inability to identify and distinguish ones own feelings. We assessed this inability using alexithymia and empathy questionnaires, and used fMRI to investigate brain activity while introspecting on emotion. Individuals with high functioning autism/Asperger syndrome (HFA/AS) were compared with matched controls. Participants rated stimuli from the International Affective Picture System twice, once according to the degree of un/pleasantness that the pictures induced, and once according to their color balance. The groups differed significantly on both alexithymia and empathy questionnaires. Alexithymia and lack of empathy were correlated, indicating a link between understanding ones own and others’ emotions. For both groups a strong relationship between questionnaire scores and brain activity was found in the anterior insula (AI), when participants were required to assess their feelings to unpleasant pictures. Regardless of self-reported degree of emotional awareness, individuals with HFA/AS differed from controls when required to introspect on their feelings by showing reduced activation in self-reflection/mentalizing regions. Thus, we conclude that difficulties in emotional awareness are related to hypoactivity in AI in both individuals with HFA/AS and controls, and that the particular difficulties in emotional awareness in individuals with HFA/AS are not related to their impairments in self-reflection/mentalizing.

Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain.

In this study, we tested the validity of 2 popular assumptions about empathy: (a) empathy can be enhanced by oxytocin, a neuropeptide known to be crucial in affiliative behavior, and (b) individual differences in prosocial behavior are positively associated with empathic brain responses. To do so, we measured brain activity in a double-blind placebo-controlled study of 20 male participants either receiving painful stimulation to their own hand (self condition) or observing their female partner receiving painful stimulation to her hand (other condition). Prosocial behavior was measured using a monetary economic interaction game with which participants classified as prosocial (N = 12) or selfish (N = 6), depending on whether they cooperated with another player. Empathy-relevant brain activation (anterior insula) was neither enhanced by oxytocin nor positively associated with prosocial behavior. However, oxytocin reduced amygdala activation when participants received painful stimulation themselves (in the nonsocial condition). Surprisingly, this effect was driven by “selfish” participants. The results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their actions being determined by their feeling anxious rather than by reason.

Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults

Theory of Mind (ToM) is the ability to attribute thoughts, intentions and beliefs to others. This involves component processes, including cognitive perspective taking (cognitive ToM) and understanding emotions (affective ToM). This study assessed the distinction and overlap of neural processes involved in these respective components, and also investigated their development between adolescence and adulthood. While data suggest that ToM develops between adolescence and adulthood, these populations have not been compared on cognitive and affective ToM domains. Using fMRI with 15 adolescent (aged 11-16 years) and 15 adult (aged 24-40 years) males, we assessed neural responses during cartoon vignettes requiring cognitive ToM, affective ToM or physical causality comprehension (control). An additional aim was to explore relationships between fMRI data and self-reported empathy. Both cognitive and affective ToM conditions were associated with neural responses in the classic ToM network across both groups, although only affective ToM recruited medial/ventromedial PFC (mPFC/vmPFC). Adolescents additionally activated vmPFC more than did adults during affective ToM. The specificity of the mPFC/vmPFC response during affective ToM supports evidence from lesion studies suggesting that vmPFC may integrate affective information during ToM. Furthermore, the differential neural response in vmPFC between adult and adolescent groups indicates developmental changes in affective ToM processing.

Attention does not modulate neural responses to social stimuli in autism spectrum disorders

We investigated whether individuals with autism spectrum disorders (ASD) would show attentional modulation for social (face) and non-social (house) stimuli. Sixteen individuals with ASD and 16 matched control participants completed a task in which pairs of face and house stimuli were present on every trial, with one of the pairs randomly assigned to attended locations and the other to unattended locations. Both mass-univariate (SPM) and region of interest analyses suggested that responses to houses were modulated by attention in both groups, but that only the control participants demonstrated attentional modulation of face-selective regions. Thus, the participants with ASD demonstrated a lack of attentional modulation which was particularly evident for the social stimulus. Analyses of effective connectivity indicated that these results were due to a failure of attention to modulate connectivity between extrastriate areas and V1. We discuss how these results may suggest a mechanism to explain the reduced salience of social stimuli in ASD.

Intact automatic imitation of human and robot actions in autism spectrum disorders

The existence of a specialized imitation module in humans is hotly debated. Studies suggesting a specific imitation impairment in individuals with autism spectrum disorders (ASD) support a modular view. However, the voluntary imitation tasks used in these studies (which require socio-cognitive abilities in addition to imitation for successful performance) cannot support claims of a specific impairment. Accordingly, an automatic imitation paradigm (a ‘cleaner’ measure of imitative ability) was used to assess the imitative ability of 16 adults with ASD and 16 non-autistic matched control participants. Participants performed a prespecified hand action in response to observed hand actions performed either by a human or a robotic hand. On compatible trials the stimulus and response actions matched, while on incompatible trials the two actions did not match. Replicating previous findings, the Control group showed an automatic imitation effect: responses on compatible trials were faster than those on incompatible trials. This effect was greater when responses were made to human than to robotic actions (‘animacy bias’). The ASD group also showed an automatic imitation effect and a larger animacy bias than the Control group. We discuss these findings with reference to the literature on imitation in ASD and theories of imitation.

Mixed emotions: the contribution of alexithymia to the emotional symptoms of autism

It is widely accepted that autism is associated with disordered emotion processing and, in particular, with deficits of emotional reciprocity such as impaired emotion recognition and reduced empathy. However, a close examination of the literature reveals wide heterogeneity within the autistic population with respect to emotional competence. Here we argue that, where observed, emotional impairments are due to alexithymia—a condition that frequently co-occurs with autism—rather than a feature of autism per se. Alexithymia is a condition characterized by a reduced ability to identify and describe one’s own emotion, but which results in reduced empathy and an impaired ability to recognize the emotions of others. We briefly review studies of emotion processing in alexithymia, and in autism, before describing a recent series of studies directly testing this ‘alexithymia hypothesis’. If found to be correct, the alexithymia hypothesis has wide-reaching implications for the study of autism, and how we might best support subgroups of autistic individuals with, and without, accompanying alexithymia. Finally, we note the presence of elevated rates of alexithymia, and inconsistent reports of emotional impairments, in eating disorders, schizophrenia, substance abuse, Parkinson’s Disease, multiple sclerosis and anxiety disorders. We speculate that examining the contribution of alexithymia to the emotional symptoms of these disorders may bear fruit in the same way that it is starting to do in autism.

Development during adolescence of the neural processing of social emotion

In this fMRI study, we investigated the development between adolescence and adulthood of the neural processing of social emotions. Unlike basic emotions (such as disgust and fear), social emotions (such as guilt and embarrassment) require the representation of anothers mental states. Nineteen adolescents (10–18 years) and 10 adults (22–32 years) were scanned while thinking about scenarios featuring either social or basic emotions. In both age groups, the anterior rostral medial prefrontal cortex (MPFC) was activated during social versus basic emotion. However, adolescents activated a lateral part of the MPFC for social versus basic emotions, whereas adults did not. Relative to adolescents, adults showed higher activity in the left temporal pole for social versus basic emotions. These results show that, although the MPFC is activated during social emotion in both adults and adolescents, adolescents recruit anterior (MPFC) regions more than do adults, and adults recruit posterior (temporal) regions more than do adolescents.

Heightened neural reactivity to threat in child victims of family violence

Summary Exposure to family violence affects a significant minority of children: estimates of physical abuse range from 4 to 16%, while intimate partner violence affects between 8 and 25% of children [1]. These maltreatment experiences represent a form of environmental stress that significantly increases risk of later psychopathology, including anxiety [1,2]. To date, no functional magnetic resonance imaging (fMRI) studies have probed the neural correlates of emotional processing in children exposed to family violence. Previous psychological and electrophysiological studies indicate a selective hypervigilance to angry cues in physically abused children, which is in turn associated with elevated levels of anxiety [3]. Functional magnetic resonance imaging (fMRI) research has demonstrated increased reactivity of the anterior insula (AI) and amygdala to angry faces in individuals with anxiety disorder [4], and in psychiatrically healthy soldiers exposed to combat [5], making these regions plausible neural candidates for adaptation to threat. We demonstrated that children exposed to family violence (with normative levels of anxiety) show increased AI and amygdala reactivity in response to angry but not sad faces. While such enhanced reactivity to a biologically salient threat cue may represent an adaptive response to sustained environmental danger, it may also constitute a latent neurobiological risk factor increasing vulnerability to psychopathology.

Through the looking glass: Counter-mirror activation following incompatible sensorimotor learning

The mirror system, comprising cortical areas that allow the actions of others to be represented in the observer’s own motor system, is thought to be crucial for the development of social cognition in humans. Despite the importance of the human mirror system, little is known about its origins. We investigated the role of sensorimotor experience in the development of the mirror system. Functional magnetic resonance imaging was used to measure neural responses to observed hand and foot actions following one of two types of training. During training, participants in the Compatible (control) group made mirror responses to observed actions (hand responses were made to hand stimuli and foot responses to foot stimuli), whereas the Incompatible group made counter‐mirror responses (hand to foot and foot to hand). Comparison of these groups revealed that, after training to respond in a counter‐mirror fashion, the relative action observation properties of the mirror system were reversed; areas that showed greater responses to observation of hand actions in the Compatible group responded more strongly to observation of foot actions in the Incompatible group. These results suggest that, rather than being innate or the product of unimodal visual or motor experience, the mirror properties of the mirror system are acquired through sensorimotor learning.