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The Neurodevelopment of Empathy in Human
The Neurodevelopment of Empathy in Human
The Neurodevelopment of Empathy in Human
Fig. 1. Schematic illustration of the macrocomponents involved in tain several perspectives and a decoupling mechanism between
human empathy. These different components are intertwined and first-person and second-person information. Emotion regulation:
contribute to different aspects of the experience of empathy. They enables the control of emotion, affect, drive and motivation. This
can be dissociated by brain lesions. Affective arousal: first com- component develops throughout childhood and adolescence, and
ponent in place in development having evolved to differentiate parallels the maturation of execution functions. The dorsolateral
hostile from hospitable stimuli and to organize adaptive respons- PFC, the anterior cingulate cortex (ACC) and the vmPFC, via
es to these stimuli. This component refers to the automatic dis- their reciprocal connections with the amygdala and widespread
crimination of a stimulus – or features of a stimulus – as appetitive cortical areas including the STS, play a primary role in self-regu-
or aversive, hostile or hospitable, pleasant or unpleasant, threaten- lation. Humans also have the capacity to appraise and reappraise
ing or nurturing. Subcortical circuits including the amygdala, hy- emotions and feelings. Thus, empathy is not a passive affective
pothalamus, hippocampus and orbitofrontal cortex (OFC) are the resonance phenomenon with the emotions of others. Rather,
essential neural components of affective arousal. The amygdala goals, intentions, context and motivations play feed-forward roles
and OFC with reciprocal connection with the superior temporal in how emotions are perceived and experienced. From this model,
sulcus (STS) underlie rapid and prioritized processing of the emo- it is clear that empathy is implemented by a complex network of
tion signal. Emotion understanding: develops later, and begins to distributed, often recursively connected, interacting neural re-
be really mature around the age of 2–3 years. This component gions (STS, insula, mPFC and vmPFC, amygdala and ACC) as
largely overlaps with theory-of-mind-like processing and draws well as autonomic and neuroendocrine processes implicated in
on the ventromedial (vm) and medial (m) prefrontal cortex (PFC) social behaviors and emotional states.
as well as executive functions. The latter allow the child to enter-
theory of empathy requires the specification of various amocingulate division of the forebrain is believed to have
causal mechanisms producing some outcome variable evolved in parallel with social behaviors related to the
(e.g. helping behavior), the moderator variables (e.g. im- perception of emotional information involved in secur-
plicit attitudes, ingroup/outgroup processes) that influ- ing emotional bonding and social interactions [MacLean,
ence the conditions under which each of these mecha- 1987]. However, humans are special in the sense that
nisms operate, and the unique consequences resulting high-level cognitive abilities such as executive function,
from each of them. language and theory of mind (ToM) are layered on top of
Empathy is not unique to humans as many of the phys- phylogenetically older social and emotional capacities.
iological mechanisms are shared with other mammalian These evolutionarily newer aspects of information pro-
species. Recognizing and evaluating signals of distress cessing expand the range of behaviors that can be driven
from newborns and infants is of primary importance in by empathy (like caring for and helping outgroup mem-
parental care for offspring survival and fitness. The thal- bers or even individuals from different species).
100
Pain CS
90
Pain CO
80 Linear (pain CS)
60 3 Signal response
in amygdala
50
40 Age (weeks)
0
30
20
10
0 –5
0 500 1,000 1,500 2,000 2,500
a Age (weeks) c
Fig. 2. a Subjective ratings of dynamic visual stimuli depicting p ! 0.05). Further, while on average participants rated the pain
painful situations accidentally caused by self (Pain CS) and pain- caused intentionally (Pain CO) conditions as significantly more
ful situations intentionally caused by another individual (Pain painful than when pain was accidentally caused by self (Pain CS;
CO) across age (in weeks) in 57 participants (from 7 to 40 years t56 = 2.581; p ! 0.01), this effect was not driven by age. b Bilateral
old). A gradual decrease in the subjective evaluation of pain in- amygdala activation. c Significant negative correlation between
tensity for both painful conditions was found across age, with age and degree of activation in the amygdala when the partici-
younger participants rating them significantly higher than older pants are exposed to painful situations accidentally caused.
participants (Pain CS: r = –0.327, p ! 0.01; Pain CO: r = –0.267, Adapted from Decety and Michalska [2010].
tor area were recruited when they watched painful, acci- homeostatic information such as pain, temperature, hun-
dentally caused situations. While participants’ subjective ger, thirst, itch and cardiorespiratory activity. It serves as
ratings of the painful situations decreased with age and a primary sensory cortex for each of these distinct intero-
were significantly correlated with hemodynamic re- ceptive feelings from the body. The posterior part has
sponse in the mPFC, increases in pain ratings were cor- been shown to be associated with interoception due to its
related with bilateral amygdala activation (fig. 2). intimate connections with the amygdala, hypothalamus,
A significant negative correlation between age and de- ACC and OFC [Jackson et al., 2006]. It has been proposed
gree of activation was found in the posterior insula. In that the right anterior insula serves to compute a higher-
contrast, a positive correlation was found in the anterior order metarepresentation of the primary interoceptive
portion of the insula. This posterior-to-anterior progres- activity, which is related to the feeling of pain and its emo-
sion of increasingly complex re-representations in the tional awareness [Craig, 2003]. In line with evidence that
human insula is thought to provide a foundation for the regulatory mechanisms continue into late adolescence
sequential integration of the individual homeostatic con- and early adulthood, greater signal change with increas-
dition with one’s sensory environment and motivational ing age was found in the prefrontal regions involved in
condition [Craig, 2004]. The posterior insula receives in- cognitive control and response inhibition, such as the
puts from the ventromedial nucleus of the thalamus, dlPFC and inferior frontal gyrus [Swick et al., 2008].
which is highly specialized for conveying emotional and Overall, this pattern of age-related change in the amyg-
dala, insula and PFC can be interpreted in terms of the ternal environment; the other subsystem, situated medi-
frontalization of inhibitory capacity, hypothesized to ally, preferentially processes interoceptive information
provide a greater top-down modulation of activity within such as visceromotor output critical for the analysis of the
more primitive emotion-processing regions [Yurgelun- affective significance of stimuli.
Todd, 2007]. Another important age-related change was In sum, the behavioral evaluations of others in distress
detected in the vmPFC/OFC: activation in the OFC in combined with the pattern of brain activation from child-
response to pain inflicted by another shifted from its me- hood to adulthood reflect a gradual change from a vis-
dial portion in young participants to the lateral portion ceral emotional response critical for the analysis of the
in older participants (fig. 3). affective significance of stimuli to a more evaluative
The medial OFC appears integral to guiding visceral function mediated by different aspects of the vmPFC and
and motor responses, whereas the lateral OFC integrates its reciprocal connections with the amygdala.
the external sensory features of a stimulus with its impact
on the homeostatic state of the body. The pattern of de-
velopmental change in the OFC seems to reflect a gradu- Conclusion
al shift between the monitoring of somatovisceral re-
sponses in young children, mediated by the medial aspect Given the importance of empathy for healthy psycho-
of the OFC, and the executive control of emotion process- logical and social interaction, it is clear that a neuro-
ing implemented by its lateral portion in older partici- developmental approach to elucidate the computational
pants. These data support the suggestion that the vmPFC mechanisms underlying affective reactivity, emotion un-
contains two feedback-processing systems, consistent derstanding and regulation is essential to complement
with hypotheses derived from anatomical studies [Hurli- traditional behavioral methods and gain a better under-
man et al., 2005]. One subsystem, situated laterally in the standing of how deficits may arise in the context of devel-
OFC, preferentially processes information from the ex- opment. Breaking down empathy and related phenomena
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