doi:10.1093/brain/awt364
Brain 2014: 137; 1–3
| e272
BRAIN
A JOURNAL OF NEUROLOGY
LETTER TO THE EDITOR
Spontaneous versus deliberate vicarious representations: different routes to empathy in
psychopathy and autism
Steven M. Gillespie,1 Joseph P. McCleery1,2 and Lindsay M. Oberman3
1 School of Psychology, University of Birmingham, Birmingham, B15 2TT, UK
2 Centre for Autism Research, Children’s Hospital of Philadelphia, PA 19104, USA
3 Department of Neurology, Beth Israel Deaconess Medical Centre, Boston, MA 02215, USA
Correspondence to: Steven M. Gillespie,
School of Psychology,
University of Birmingham,
Edgbaston, Birmingham, B15 2TT, UK
E-mail: [email protected]
Sir, We read the article recently published by Meffert et al. (2013)
with great interest. The authors used functional MRI to investigate
vicarious emotional representation in psychopathic offenders,
scanning 18 psychopaths and 26 non-offending control subjects.
Participants were either presented with video clips of short emotional interactions or experienced similar interactions themselves.
Results showed that although psychopaths showed normal patterns of neural activation in response to experience, abnormal patterns of activation were observed during observation of others’
interactions in those regions known to be involved in vicarious
emotional experience. However, when participants were instructed
to ‘feel with the hands in the videos’ differences in activation
between psychopaths and control subjects were significantly
reduced in numerous regions of interest, including the medial
and anterior left insula, left anterior cingulate cortex, and bilateral
angular gyri (Meffert et al., 2013). The authors conclude that
these results point toward reduced spontaneous but intact deliberate vicarious representations in psychopathy.
Psychopathy represents a severe disorder of personality, characterized by a callous lack of empathy, shallow affect, and a lack of
remorse or guilt (Hare, 1991, 2003). Traditional theories have
emphasized poor recognition of others’ distress cues, including emotional facial expressions, as central to empathy deficits observed in
psychopathy (Blair et al., 2001, 2004; Montagne et al., 2005; Dadds
et al., 2006; Dolan and Fullam, 2006; see also meta-analyses by
Marsh and Blair, 2008; Wilson et al., 2011). These findings are extended through the more recent results of Meffert et al. (2013),
which suggest that psychopaths may exhibit a particular breakdown
in the neural processes that underlie the spontaneous vicarious experience of the emotions of others. Thus, Meffert et al. (2013)
findings add significantly to current understanding of empathy deficits in psychopathy, distinguishing between spontaneous and deliberate vicarious experience.
We were drawn to write a letter in response to the publication
of this article because of a related line of research on individuals
with autism spectrum disorder (ASD). Similar to those with psychopathy, research suggests that individuals with ASD often exhibit
difficulties in the processing of emotional expressions (Hall et al.,
2007; Clark et al., 2008). However, similar to the findings by
Meffert et al. (2013), studies have indicated that there may also
be a dissociation between spontaneous and deliberate experience
in this population. For example, adults with Asperger syndrome
can understand mental states such as desires and beliefs
(mentalizing) when explicitly prompted to do so, despite having
impairments in this domain during spontaneous tasks (Senju et al.,
2009). Additionally, two studies have shown impaired spontaneous but intact deliberate empathic motor mimicry in ASD
(McIntosh et al., 2006; Oberman et al., 2009).
The mechanisms underlying impaired empathic responding in
autism and psychopathy appear to differ. Emotion recognition deficits in psychopathy are thought to be the result of amygdala
hypoactivity, and are believed to be at the core of psychopaths’
callous lack of empathy (Blair, 2007). Alternatively, similar findings
in ASD may stem from more general impairments in the processing of facial stimuli, including abnormal functioning of the fusiform
face area in the fusiform gyrus (Critchley et al., 2000; Pierce et al.,
2001; Dalton et al., 2005), an essential structure for the cognitive
representation of facial stimuli.
Relevant to the Meffert et al. (2013) findings, several recent
studies have examined the role of personal familiarity on the
Advance Access publication January 28, 2014
ß The Author (2014). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved.
For Permissions, please email: [email protected]
e272
| Brain 2014: 137; 1–3
activation of neural mechanisms involved in both social and empathy-related processing in ASD. For example, Pierce and Redcay
(2008) used functional MRI to examine regions of interest including the amygdala, fusiform gyrus, and anterior and posterior anterior cingulate cortices in children with ASD while they viewed
pictures of the faces of (i) a familiar adult; (ii) a stranger adult; (iii)
a familiar child; and (iv) a stranger child. While fusiform activity in
response to the face of an adult stranger was strikingly absent in
the children with ASD, the results also revealed normal fusiform
activity while these children viewed both their mother’s face and
the faces of other children (Pierce and Redcay, 2008). These results strongly suggest a role for a social-emotional connection in
mediating the activation of the social perception system in those
with ASD.
The importance of social-emotional relevance in autism was further demonstrated by Oberman et al. (2008). In this study we
presented video clips of both familiar and non-familiar actors
performing grasping actions to children with ASD and control children, while recording EEG activity (Oberman et al., 2008).
Analysis of EEG mu suppression, a putative marker of ‘mirror
neuron’ functioning, revealed that children with ASD exhibited
relatively intact mu suppression during the observation of the actions of people familiar to them but impaired mu suppression
during the observation of the same actions of unfamiliar people.
We interpreted these data as evidence that mirror neuron system
activation is also modulated by the social-emotional significance of
the observed individual to the person with autism (Oberman
et al., 2008).
Taken together, these findings suggest that individuals with ASD
exhibit relatively more intact social and empathic activations when
the observed individuals are socially and emotionally relevant to
them, or when they are given explicit instructions to do so. On the
other hand, the spontaneous activation of these same social and
empathic mechanisms is commonly and distinctly reduced or
absent during the observation of individuals unknown to them.
This pattern of results contrasts with the findings Meffert et al.
(2013) observed in individuals with psychopathy. In these individuals, social brain regions were active under both spontaneous and
deliberate conditions, whereas the activation of neural mechanisms
involved specifically in empathy were active only under deliberate
instruction.
The finding that psychopaths fail to spontaneously activate the
empathic system despite intact social-cognitive representations
and activations may account for the callous lack of empathy characteristic of psychopaths’ antisocial behaviours, including a proclivity toward instrumental, premeditated, and goal-directed acts of
aggression (Cornell et al., 1996; Woodworth and Porter, 2002).
Alternatively, individuals with ASD seem to activate neither the
social nor the empathic system (e.g. when observing individuals
of little to no social or emotional relevance to them), or to activate
both the social and the empathic systems (e.g. when observing
individuals of clear social and emotional relevance to them). This
pattern of findings may account for the fact that, although individuals with ASD commonly fail to respond to both the social and
emotional overtures of others, there is very little to no evidence to
suggest that these individuals actively exhibit elevated levels of
proactive aggression. Indeed, research shows that children with
Letter to the Editor
ASD are actually more likely to report being victims of bullying
(Little, 2002; Wainscot et al., 2008; Carter, 2009; Kloosterman
et al., 2013), which may represent one form of proactive aggression (Camodeca et al., 2002). That is to suggest that the key
distinction between those with ASD and those with psychopathy
may be that the activation of social and empathic systems and
associated mechanisms are more tightly linked in individuals with
ASD than in individuals with psychopathy, and that the preservation of this link in those with ASD may explain their aloof but
non-malicious behavioural phenotype relative to those with
psychopathy.
These results may have implications for the development of
interventions that aim to improve social communication in autism
and empathic functioning in psychopathy. For example, interventions in autism may seek to increase the extent to which the individual identifies with, or assigns personal significance to, unfamiliar
others. This may in turn lead to increases in both empathic responding and improved social communication. For example, Bölte
et al. (2006) showed that the use of a computer-based program
led to significant improvements in the recognition of basic emotional expressions in individuals with ASD that were linked to
changes in neural activity in the superior parietal lobe and the
medial occipital gyrus (Bolte et al., 2006). These results suggest
that improvements in emotion recognition in autism are dependent
upon improved processing of facial stimuli, rather than an improved ability to recognize emotional expressions per se.
Similar interventions have also been undertaken in an effort to
address expression recognition deficits in psychopathy. For example, Dadds et al. (2006, 2008) found that children with callous
unemotional traits showed improved performance when asked to
specifically focus attention on the eyes of emotionally expressive
faces. Furthermore, Dadds et al. (2012) have shown that a randomized controlled trial of emotion recognition training led to
improvements in empathy and conduct problems among children
with high callous-unemotional traits. However, these results do
not necessarily indicate an increased capacity to ‘experience’ the
emotions of others. The use of neurophysiological recordings in
future research may eventually add weight to the argument that
such interventions can improve emotional empathy. However, it
should also be noted that such physiological changes may not be
interpreted in the same way among psychopathic individuals compared with healthy control subjects. Thus, while the results of
Dadds et al. (2012) and Meffert et al. (2013) represent critically
valuable and important steps toward therapeutic intervention in
psychopathy, the experiential or emotional correlates of such
changes, as yet, remain unknown.
References
Blair RJ. The amygdala and ventromedial prefrontal cortex in morality
and psychopathy. Trends Cogn Sci 2007; 11: 387–92.
Blair RJ, Colledge E, Murray L, Mitchell DG. A selective impairment in
the processing of sad and fearful expressions in children with psychopathic tendencies. J Abnorm Child Psychol 2001; 29: 491–8.
Blair RJ, Mitchell DGV, Peschardt KS, Colledge E, Leonard RA, Shine JH,
et al. Reduced sensitivity to others’ fearful expressions in psychopathic
individuals. Pers Indiv Differ 2004; 37: 1111–22.
Letter to the Editor
Bölte S, Hubl D, Feineis-Matthews S, Prvulovic D, Dierks T, Poustka F.
Facial affect recognition training in autism: can we animate the fusiform gyrus? Behav Neurosci 2006; 120: 211–16.
Camodeca M, Goossens FA, Terwogt MM, Schuengel C. Bullying and
victimization among school-age children: stability and links to proactive and reactive aggression. Soc Dev 2002; 11: 332–45.
Carter S. Bullying of students with Asperger Syndrome. Issues Compr
Pediatr Nurs 2009; 32: 145–54.
Clark TF, Winkielman P, McIntosh DN. Autism and the extraction of
emotion from briefly presented facial expressions: stumbling at the
first step of empathy. Emotion 2008; 8: 803–9.
Cornell DG, Warren J, Hawk G, Stafford E, Oram G, Pine D.
Psychopathy in instrumental and reactive violent offenders. J Consult
Clin Psychol 1996; 64: 783–90.
Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T,
Robertson DM, et al. The functional neuroanatomy of social behaviour
changes in cerebral blood flow when people with autistic disorder
process facial expressions. Brain 2000; 123: 2203–12.
Dadds MR, El Masry Y, Wimalaweera S, Guastella AJ. Reduced eye gaze
explains ‘fear blindness’ in childhood psychopathic traits. J Am Acad
Child Adolesc Psychiatry 2008; 47: 455–63.
Dadds MR, Cauchi AJ, Wimalaweera S, Hawes DJ, Brennan J. Outcomes,
moderators, and mediators of empathic-emotion recognition training
for complex conduct problems in childhood. Psychiat Res 2012; 199:
201–7.
Dadds MR, Perry Y, Hawes DJ, Merz S, Riddell AC, Haines DJ, et al.
Attention to the eyes and fear-recognition deficits in child psychopathy. Br J Psychiat 2006; 189: 280–1.
Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA,
Goldsmith HH, et al. Gaze fixation and the neural circuitry of face
processing in autism. Nat Neurosci 2005; 8: 519–26.
Dolan M, Fullam R. Face affect recognition deficits in personality-disordered offenders: association with psychopathy. Psychol Med 2006;
36: 1563–70.
Hall GB, West CD, Szatmari P. Backward masking: evidence of reduced
subcortical amygdala engagement in autism. Brain Cogn 2007; 65:
100–6.
Hare RD. The Hare psychopathy checklist—revised. North Tonawanda,
NY: Multi-Health Systems; 1991.
Hare RD. Manual for the revised psychopathy checklist. 2nd edn.
Toronto: Multi-Health Systems; 2003.
Kloosterman PH, Kelley EA, Craig WM, Parker JD, Javier C. Types and
experiences of bullying in adolescents with an autism spectrum disorder. Res Autism Spectr Disord 2013; 7: 824–32.
Brain 2014: 137; 1–3
| e272
Little L. Middle-class mothers’ perceptions of peer and sibling victimization among children with Asperger’s syndrome and nonverbal learning
disorders. Issues Compr Pediatr Nurs 2002; 25: 43–57.
Marsh AA, Blair RJ. Deficits in facial affect recognition among antisocial
populations: a meta-analysis. Neurosci Biobehav Rev 2008; 32:
454–65.
McIntosh DN, Reichmann-Decker A, Winkielman P, Wilbarger JL. When
the social mirror breaks: deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Dev Sci 2006; 9:
295–302.
Meffert H, Gazzola V, den Boer JA, Bartels AA, Keysers C. Reduced
spontaneous but relatively normal deliberate vicarious representations
in psychopathy. Brain 2013; 136: 2550–62.
Montagne B, van Honk J, Kessels RPC, Frigerio E, Burt M, van
Zandvoort MJE, et al. Reduced efficiency in recognising fear in subjects
scoring high on psychopathic personality characteristics. Pers Indiv Diff
2005; 38: 5–11.
Oberman LM, Ramachandran VS, Pineda JA. Modulation of mu suppression in children with autism spectrum disorders in response to familiar
or unfamiliar stimuli: the mirror neuron hypothesis. Neuropsychologia
2008; 46: 1558–65.
Oberman LM, Winkielman P, Ramachandran VS. Slow echo: facial EMG
evidence for the delay of spontaneous, but not voluntary, emotional
mimicry in children with autism spectrum disorders. Dev Sci 2009; 12:
510–20.
Pierce K, Redcay E. Fusiform function in children with an autism
spectrum disorder is a matter of ‘who’. Biol Psychiat 2008; 64:
552–60.
Pierce K, Müller RA, Ambrose J, Allen G, Courchesne E. Face processing
occurs outside the fusiformface area in autism: evidence from functional MRI. Brain 2001; 124: 2059–73.
Senju A, Southgate V, White S, Frith U. Mindblind eyes: an absence of
spontaneous theory of mind in Asperger syndrome. Science 2009;
325: 883–5.
Wainscot JJ, Naylor P, Sutcliffe P, Tantam D, Williams JV. Relationships with
peers and use of the school environment of mainstream secondary school
pupils with Asperger Syndrome (High-Functioning Autism): a case-control study. Int J Psychol Psychol Ther 2008; 8: 25–38.
Wilson K, Juodis M, Porter S. Fear and loathing in psychopaths: a metaanalytic investigation of the facial affect recognition deficit. Crim
Justice Behav 2011; 38: 659–68.
Woodworth M, Porter S. In cold blood: characteristics of criminal homicides as a function of psychopathy. J Abnorm Psychol 2002; 111:
436–45.