Understanding Emotions
in Others: Mirror Neuron
Dysfunction in Children
with Autism Spectrum
Disorders
Mirella Depretto, Mari S. Davies, Jennifer H. Pfeifer, Ashley A. Scott,
Marian Sigman, Susan Y. Bookheimer, & Marco Iacoboni
Published online 4 December 2005. Nature Neuroscience. Volume 9,
Number 1, January 2006. Nature Publishing Group.
Summarized by Shannon Juedes
Autism Spectrum Disorders
http://www.nimh.nih.gov/publicat/autism.cfm
• A recent study of a U.S. metropolitan area estimated that 3.4 of
every 1,000 children 3-10 years old had autism.
• ASD is often dismissed. The child is just a little slow and “will
catch up.”
• All children with ASD demonstrate deficits in
–
–
–
–
1) social interaction
2) verbal and nonverbal communication
3) repetitive behaviors or interests.
In addition, they will often have unusual responses to sensory
experiences, such as certain sounds or the way objects look.
– Each of these symptoms runs the gamut from mild to severe. They
will present in each individual child differently.
Autism Spectrum Disorder
(Cont.)
http://www.nimh.nih.gov/publicat/autism.cfm
• Postmortem and MRI studies have
shown that many major brain structures
are implicated in autism.
• Other research is focusing on the role of
neurotransmitters such as serotonin,
dopamine, and epinephrine.
Mirror Neurons
• Rizzolatti et al. found that neurons in an area of the
rostral part of the ventral premotor cortex in the
monkey brain became active when monkeys saw
people or other monkeys perform various movements
or when they performed these movements
themselves. These neurons were also found in the
inferior parietal lobule which is connected with the
ventral premotor cortex.
– Mirror neuron system activity in the human homolog of area
F5—the pars opercularis in the inferior frontal gyrus—has
been consistently reported during imitation, action
observation, and intention understanding.
• Mirror Neurons: Neurons located in the ventral
premotor cortex and inferior parietal lobule that
respond when the individual makes a particular
movement or sees another individual making that
movement.
Mirror Neurons
• The “What” System—recognition of objects involves the ventral
stream of the visual association cortex including the inferior
temporal cortex
• The “Where” System—perception of location and movement
involves the dorsal stream of the posterior parietal cortex. This
system includes the mirror neuron circuit (The “How” system.)
• The “Why” System—The Intent of the Action/Mediation of
Understanding of Emotional States of Others
– “[A]n action is understood when its observation causes the
motor system of the observer to ‘resonate.’ So, when we
observe a hand grasping an apple, the same population of
neurons that control the execution of grasping movements
becomes active in the observer’s motor areas…In other
words, we understand an action because the motor
representation of that action is activated in our brain.”
• The neurons responded to either the sight or the execution of
particular movements.
– Sight and Sound
Prelude
• Dysfunction of the mirror neuron system (MNS) early
in development could give rise to the cascade of
impairments that are characteristic of ASD.
• Using fMRI, a neural network in which the insula acts
as an interface between the frontal component of the
MNS and the limbic system was described, thus
enabling the translation of an observed or imitated
facial emotional expression into its internally felt
emotional significance.
Previous Studies
• Three recent studies used different
electrophysiological techniques have each
reported preliminary evidence for abnormal
MNS functioning during action imitation and
observation in adults with ASD.
• A more definitive test of MNS theory of autism
would involve examining MNS activity in the
content of a socio-emotional task and in a
sample of children.
The Experiment
• An event-related fMRI design was used to
investigate neural activity during the imitation
and observation of facial emotional
expressions.
• Subjects:
– 9 high-functioning children with ASD (12.05+/- 2.50
years)
– 9 typically-developing children matched by age and
IQ (12.38+/- 2.22 years)
The Experiment (Cont.)
• Stimuli:
– 80 faces expressing five different emotions:
• Anger, Fear, Happiness, Neutrality, or Sadness
• Presented for two seconds with optimized
random sequence that included null events
(blank screens with fixation crosses at eye level)
and temporal jittering to increase statistical
efficacy
The Experiment (Cont.)
• In two separate scans (with the order counterbalanced
within each group), subjects either imitated or simply
observed the faces via high-resolution, magnetcompatible goggles.
• All children practiced the tasks outside the scanner to
demonstrate that they were willing and able to comply
with the task requirements.
• Half the children in each group also performed both
tasks during a video-taped session with an eye
tracker.
Observations
• Imitation of Emotional Expressions vs. Null Events:
– The typically developing children activated a neural network
very similar to that previously observed in adults.
• Extensive bilateral activation of striate and extra striate cortices,
primary motor and premotor regions, limbic structures
(amygdala, insula, and ventral striatum) and the cerebellum.
– Showed strong bilateral activity within the pars opercularis of
the inferior frontal gyrus (Brodmann’s area 44) as well as in
the neighboring pars triangularis (Brodmann’s area 45), with
strongest peaks in the right hemisphere.
Observations (Cont.)
• Observations of the ASD group:
– Robust activation in visual cortices,
premotor and motor regions of the face and
the amygdala.
• Indicates that these children attend to the stimuli
and imitated the facial expressions.
– Failed to show any activity in the mirror area
in the pars opercularis
Observations (Cont.)
• Direct Comparisions between the ASD group and the
typically developing children confirmed that activity in
the anterior component of the MNS was reliably
greater in typically developing children.
• TD children showed reliably greater activity in insular
and periamygdaloid regions as well as in the ventral
striatum and thalamus.
• ASD children showed greater activity in left anterior
parietal and right visual association areas.
Findings
• Individuals with ASD typically show deficits in
understanding the emotional states of others.
– Dysfunction in the MNS should be manifest not only
when these individuals imitate emotional
expressions but when they observe others’
emotions
• Activity in the right pars opercularis during the observation
of facial expressions was stronger in the TD group then
the ASD group
• Difference is not attributed to the failure of the children
with ASD to attend to the face stimuli as both groups
showed activation in regions implicated in face processing.
To Further Test the Hypothesis:
• Examined the relationship between
activity in regions with MN properties and
symptom severity, as indexed by
children’s scores on the ADOS-G and
the ADI-R.
• Controlled for IQ
Observations
• Negative correlations between activity in the
pars opercularis and the children’s scores on
the social subscales of the ADOS-G and ADIR.
– The greater the activity in this critical component of
the MNS during imitation, the higher a child’s level
of functioning in the social domain
– Activity in components of the normative network
underlying emotion understanding via action
representation was also negatively correlated with
symptom severity.
Analysis of Experiment
•
Although they were unable to monitor gaze fixation
during scanning, a variable shown to affect brain
activity in ASD, it is unlikely that their findings reflect
between-group differences in the amount of time
spent looking at the eye region.
1. During neither the imitation or observation of
facial expressions did they find group differences
in the fusiform region.
2. Activity in the fusiform gyrus did not correlate with
activity in MNS areas in either condition.
3. In the children with ASD for whom eye-tracking
data were available, there was no indication of a
positive relationship between MNS activity in the
pars opercularis and time spent fixating the eyes.
Analysis of the Experiment
(Cont.)
•
Despite the fact that they were unable to monitor task
performance during scanning and imitation deficits in ASD, they
believe that their findings reflect the children with ASD not
performing the imitation task or not performing it well.
1. All the children were willing and able to perform the task
before scanning.
2. Children with ASD performed the task outside the scanner
as well as TD children.
3. Observations of the ASD group show robust activity in
primary motor and premotor areas of the face during the
imitation task, with no evidence of between group
differences in these regions.
4. The ASD children showed greater activity than the typically
developing children in right visual and left anterior parietal
areas.
Conclusions
• The neural strategies adopted by the TD and
ASD groups are quite different.
– TD children rely upon a right hemisphere-mirroring
neural mechanism—interfacing with the limbic
system via the insula.
– ASD children must adopt an alternative strategy of
increased visual and motor attention. In effect, the
internally felt emotional significance of the imitated
facial expression is not probably not experienced.
Conclusions (Cont.)
• The fact that TD children showed increased MNS
activity even when simply observing an emotional
expression indicates that this mirroring mechanism
underlies the ability to read others’ emotional states
from a glance.
• The lack of MNS activity during both the imitation and
the observation of emotional expressions in their
sample of children with ASD provides support that
early dysfunction in the MNS may be at the core of the
social deficits that are typical of ASD.