Mirror Neurons
Michael A. Arbib
arbib@usc.edu
University of Southern California Brain Project
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A Different Methodology from Imaging Genetics
Computational Cognitive and Social Neuroscience
Computational models of neural networks (structured by brain regions)
Descending influences
of evolved extensions
on basic homologues
homology
monkey
human
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Williams, J. H., Whiten, A., Suddendorf, T. & Perrett, D. I. (2001)
Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25(4)
They hypothesize: The clinical syndrome of autism may result from a
cascade of developmental impairments emerging from
early developmental failures of mirror neuron systems
Mirror Neurons and their Dysfunction:
Just one piece of the puzzle of autism and
schizophrenia
Arbib, M.A., 2007, Autism – More than the Mirror System, Clinical
Neuropsychiatry, 4:208-222.
Arbib, M. A. & Mundhenk, T. N. (2005) Schizophrenia and the
mirror system: an essay. Neuropsychologia 43(2): 268-280
Before We Get to Autism
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Introducing AIP and F5 (Grasping) in Monkey
AIP - grasp
affordances
in parietal cortex
Hideo Sakata
F5 - grasp
commands in
premotor cortex
Giacomo Rizzolatti
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Grip Selectivity in a Single AIP Cell
A cell that is
selective for side
opposition
(Sakata)
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Grasp Specificity in an F5 Neuron
Precision pinch (top)
Power grasp (bottom)
(Data from Rizzolatti et
al.)
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The FARS Modificato Model (Fagg & Arbib, 1998)
An Implemented Computational Model
The Roles of the Dorsal (“How”) and Ventral (“What”) Streams
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Mirror Neurons
The effective observed movement
≈
The effective executed movement
STS
Rizzolatti, Fadiga
Gallese, and Fogassi
1995
Other
Self
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MNS Model of the Mirror System (Oztop & Arbib 2002)
Key idea: Learning to recognize the
trajectory relating hand to object
during a manual action
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Beyond the Mirror
•We stress the importance of
mirror neuron systems (note
plural)
• But deny that mirror neurons
do “it” (imitation, language,
prevent autism) all by
themselves
We must go “beyond the mirror”
to seek larger neural systems of
which mirror neurons are a part
Illustration by John Tenniel
From Lewis Carroll’s
Through the Looking-Glass
and what Alice found there
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Buccino et al. (2004) Neural circuits involved in the
recognition of actions performed by nonconspecifics
Buccino et al: Actions belonging to the motor repertoire of the observer (e.g.,
biting and speech reading) are mapped on the observer's motor system.
Actions that do not belong to this repertoire (e.g., barking) are recognized
based without such mapping.
Counter view: Actions belonging to the motor repertoire of the observer (e.g.,
biting and speech reading) are mapped on the observer's motor system.
All actions can be recognized without such mapping.
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Agency & Schizophrenia
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Schizophrenia: Alien Voices and Hands
Two symptoms of schizophrenia that are Problems of Agency
Auditory verbal hallucinations (AVH)
hearing another person or entity talking to him, when in fact
the schizophrenic patient is creating subvocal vocalizations, which are the
embodiment of the voices they report to hear.
Delusions of influence
The arm of the patient may move, but the patient attributes it to an external
influence.
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Daprati et al. (1997): A Study of So-Called Agency
Normal subjects and schizophrenic patients performed a requested movement with the
right hand, and observed an image of a hand movement on a video screen.
The subject was asked:
You have just seen the image of a moving hand. Was it your own hand ? Answer YES if you
saw your own hand performing the movement you have been executing. Answer NO
otherwise
The image was either of
their own hand (Subject);
the experimenter's hand performing a similar movement (Experimenter Same); or
the experimenter's hand performing a different movement (Experimenter Different).
Both normals and schizophrenics made virtually no errors when subjects saw their own
hand, or a hand performing a different movement.
The only errors occurred in the Experimenter Same condition where the median error
rate was 5/30 in the control group, 17/30 in the non-delusional group and 23/30 in the
delusional group.
Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, J. & Jeannerod, M. (1997)
Looking for the agent: an investigation into consciousness of action and self-consciousness in
schizophrenic patients. Cognition 65: 71-86.
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Agency
Daprati et al.: “These show a problem for schizophrenics in their sense of agency”
Arbib & Mundhenk: These results have nothing to do with attribution of agency!
In each case, it seems that the subject knows that s/he has made a movement and
which type of movement it is – it is a case of monitoring that movement
accurately enough to tell whether a slight variant is indeed different.
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Self-Monitoring ≠ Agency Attribution
Hypothesis: Two different factors that may affect the symptoms of
schizophrenia are self-monitoring and attribution of agency:
Self-Monitoring: Did I knock over that glass?
Agency Attribution: I see/hear hammering? Who is doing it?
We rarely recognize the agent from a hand movement alone
We usually connect the hand to a recognizable person or context
Two levels of attributing agency:
a) Self versus other: If I do not know that I acted then I believe that
someone else acted
b) Which other?: If I believe that someone else acted then I may try
to determine who the agent of the action is.
Enter the risk of confabulation
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Multiple Working Memories
Arbib and Mundhenk (2005) hypothesize that each action is accompanied
by a motor working memory of the trajectory of the action.
If the need arises to question the agency of the action, the brain
may consult its
working memories to determine:
whether there was priming of the action then disinhibition prior
to the action (normally, the basal ganglia inhibit a set of candidate
next-actions until instructed to “release” one of them);
if so, whether the working memory of expected outcome of the
action sufficiently matches the observed trajectory of the
outcome.
⇒ Only the latter invokes a mirror neuron type response – but it’s
not just “action categorization;” it also involves details of the
trajectory.
On this basis, the normal brain can decide “I’m the agent”, “I’m the agent
but the action didn’t come out as intended”, or “I’m not the agent”.
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Deficits of Disinhibition
Arbib and Mundhenk (2005) hypothesize that the primary deficit in
Auditory verbal hallucinations (AVH) and Delusions of influence
is in the lack of adequate control of disinhibition so that
an action may be committed without need for a disinhibitory signal
that represents the decision to execute the action
lacking any memory of having intended the action, the patient
concludes “I’m not the agent” and then proceeds to confabulate,
to provide an account for the agency of the observed action.
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Relevance of the MNS Model
MNS Learning:
A set of trajectories (movement and preshaping of the hand in relation to an
object’s affordances for grasping) becomes associated with the activity of specific
sets of neurons
MNS Simulation Results:
a) The model can indeed appropriately associate sets of trajectories with
classifications of actions (mirror neuron coding)
Modeling Self-Monitoring:
The results of Daprati et al. and Franck et al. (parametric analysis of Experimenter
Same) can be addressed by failure to assess small differences between working
memory of expected outcome of the intended action and the observed
trajectory of the outcome [and this requires augmenting the MNS model]
In other words, we are led to posit different failures of underlying mechanisms
for two different aspects of schizophrenia:
failures of Self-Monitoring and failures of Agency Attribution
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Anticipating Trajectories
Aglioti et al (2008) investigated the dynamics of action anticipation and its
underlying neural correlates for subjects observing free shots at a basket
in basketball.
Professional basketball players predicted the success of free shots at a basket
earlier and more accurately than did
individuals with comparable visual experience (coaches or sports journalists)
and novices.
Moreover, performance between athletes and the other groups differed
before the ball was seen to leave the model's hands, suggesting that
athletes predicted the basket shot's fate by reading body kinematics.
Both visuo-motor and visual experts showed a selective increase of motorevoked potentials during observation of basket shots.
However, only athletes showed a time-specific motor activation during
observation of erroneous basket throws.
Aglioti et al suggest that achieving excellence in sports may be related to
the fine-tuning of specific anticipatory mirror mechanisms that support the
ability to predict others' actions ahead of their realization.
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Autism
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Autistic Spectrum Disorders (ASD)
Autistic children are not impaired in:
Object permanence understanding
Tool use
Object categorization
Attachment
Self recognition
Recognition of others
But they are impaired (with differing severity depending on where
children lie on the [multi-dimensional] autism disorder “spectrum”) in:
Social interaction & communication
Play behavior
Imitation & pantomime
Emotion perception
Shared attention
Pretense
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Imitation, Mirror Neurons & Autism
Autism is often characterized by:
repetitive and stereotyped behavior (including copied behaviors)
obsessive desire for sameness
delayed and deviant language development (including echolalia) and
difficulties in executive function, perceiving or planning at high-levels of
organization.
Williams, Whiten, Suddendorf & Perrett hypothesize:
Early developmental failures of mirror neuron systems are likely to result in a
cascade of developmental impairments to yield the clinical syndrome of autism.
Williams et al. focus on a disturbance involving difficulties both
in imitating actions and
in inhibiting more stereotyped mimicking
An apparent paradox?
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Dapretto et al. 1
Stimuli consisted of 80 faces
expressing five different emotions:
anger, fear, happiness, neutrality or
sadness.
Subjects either imitated or simply
observed the faces
Activity in bilateral pars opercularis
(stronger in the right) of the inferior
frontal gyrus is seen
in the typically developing
group (a)
not in the ASD group (b).
Dapretto, M., Davies, M.S., Pfeifer, J.H., Scott, A.A., Sigman, M., Bookheimer, S.Y. & Iacoboni, M.
(2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum
disorders.
Nat Neurosci 9(1): 28-30.
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Dapretto et al. 2
BUT: There were no group differences in how well the children
imitated facial expressions
A Disturbing Thought:
The (an?) MNS isn’t important for recognition of facial expressions!!
However:
Children with ASD showed greater activity than did the typically developing
children in right visual and left anterior parietal areas
Regions shown to be modulated by visual and motor attention, respectively.
Dapretto et al. suggest that although both groups performed the imitation task
as requested, the neural strategies adopted by typically developing children and
those with ASD may be quite different
But the bigger issue is this: How do we test the implicit claim that MNS links
into a system for empathizing with emotions whereas the “autistic alternative”
does not?
Piecemeal Faces?
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A Challenge for Understanding and Intervention
Michael Rutter:
Autism research: lessons from the past and prospects for the future. J
Autism Dev Disord 35 (2005)
[Research] … has concentrated on the deficits rather than on the equally
important question of the compensatory cognitive strategies that
individuals with autism use.
[Autistic] children could and did acquire a variety of useful social,
behavioral, and communication skills but they were much better in
demonstrating these in situations comparable to those in which they
were taught, rather than through their spontaneous usage of the skills
in other situations.
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Theory of Mind
Two types of representations (Leslie, 1987) :
First-order: describe visible bodies and events.
Second-order: describe invisible minds and mental events and
serve to make sense of otherwise contradictory or incongruous
information.
The latter constitute a person’s Theory of Mind (ToM)
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Sally-Anne Task
1
..
2
..
3
..
4
..
5
..
..
..
..
Where will Sally look
for the marble?
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Polaroid photograph task
1
2
3
Where does the invisible photo show the teddy bear?
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Autism and Theory of Mind?
Baron-Cohen et al. (1985) argued that autistic children’s difficulties in
understanding the beliefs of others suggest that they lack ToM.
But such ToM does not typically become robust in normal children before
age four, yet autistic disorders are manifested earlier.
This has led some to search for ‘precursors’ to ToM, such as
pretend play and
a capacity to engage in shared attention with another individual.
Others have argued that early social deficits are often broader in scope
than implied by a focus on ToM, e.g.
the primary deficit is socio-affective, a lack of empathic and emotional
engagement with others.
But none of this explains repetitive and stereotyped behavior (including
copied behaviors), obsessive desire for sameness, delayed and deviant
language development (including echolalia), or difficulties in planning at highlevels of organization (“executive function”).
:-) .
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Adopting another’s perspective
Consider an imitation task in which the subject sees someone having their
hands linked by their thumbs and showing the palms of his hands to the
imitator.
Children with autism reproduce the effect the action had on them, rather
than the original action as performed by its agent.
Both imitation and attribution of mental states involve translating
from the perspective of another individual to oneself.
Such considerations led (Carruthers & Smith 1996, Whiten 1996) to the
hypothesis that the autistic children's beliefs are based solely on their firstorder perceptions of the world.
But the “photograph experiment” shows the autistic child can change
perspective.
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But it’s not just perspective
First-order representations describe visible bodies and events.
Second-order representations describe invisible minds and
mental events.
This omits indirect representations which describe “invisible”
events, such as internal states of objects which affect one’s
predictions about them
Mental events are a special case of indirect representations.
The crucial point of the Polaroid photograph task is that the autistic
child may form indirect representations, yet not connect them with
scenarios of the kind:
“this person is like me; if I had had the experiences they have had, then
my mental state would be different, and so what they are now thinking
will be different from what I am thinking, namely …”
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And There’s More …
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What to do with the Amygdala?
Baron-Cohen et al. (2000) The
amygdala theory of autism:
When judging from another
person’s eyes what that person
might be thinking or feeling
* patients with autism did not
activate the amygdala
* people without autism did.
Proposal: The amygdala is one of
several neural regions abnormal in
autism.
LeDoux
Amaral et al. (2003) The amygdala is not an essential component of the neural
network for social cognition:
Adult rhesus monkeys with bilateral lesions of the amygdala demonstrate near
normal social interactions with conspecifics.
The amygdala does appear to participate in the evaluation of the “safety” of social
interactions so may have a role in modulating the amount of social behavior in
which an organism will participate.
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Cerebellum & Hippocampus
Riva and Giorgi (2000): Cerebellar vermal lesions can lead to
behavioral disturbances ranging from irritability to behaviors
reminiscent of autism.
Bauman & Kemper (2005): Hippocampal lesions impair precise
representation of temporal information across a range of tasks
and would impair the construction of a time-space map of
events vital for extracting abstract structure from sequences of
events to produce second-order representations.
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Temporal Cortex
Object recognition
Causal Operations
What’ pathway
Prefrontal Cortex
Working memory
Planning
Space-time map
Parietal Cortex
Object affordances
‘How’ pathway
Hippocampus
Navigation
Declarative memory
Motor plans
Motor Cortex
.
Thalamus
Striatum
Premotor
Mirror neurons
Pons
Cerebellum
Inverse and
forward models
GPi
STN
Basal Ganglia
Memory and sequence management.
Inhibition.
1 First-order representations /
own perception
2 Current state / next state
3 Exception management /
own vs. others’ selection
4 Response reassignment /
Timing
5 Saved context / events
6 One-shot learning
7 Second-order
representations / others
BtM Overview
(Salvador Marmol 2002)
What I’ve Been Doing Lately
homology
Descending influences
of evolved extensions
on basic homologues
monkey
human
Oxford University Press, 2012
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