Download than the Mirror System - Clinical Neuropsychiatry

Clinical Neuropsychiatry (2007) 4, 5-6, 208-222
AUTISM – MORE THAN THE MIRROR SYSTEM
1
Michael A. Arbib
Abstract
A number of studies have suggested an important role for defects in mirror neurons in developmental problems
that lead to autism. My aim is to place this in perspective by
•
stressing the importance of mirror neuron systems (note plural), while
•
denying that mirror neurons do “it” (imitation, language, prevent autism) all by themselves
We must go both “within the mirror” to study the working of mirror systems in more detail and “beyond the
mirror” to study mirror neuron systems within the context of larger neural systems for imitation, empathy and language.
The present paper approaches this as follows: First, I summarize some basic characteristics of autism spectrum disorder
(ASD) and mirror neuron systems (MNSs) and then present an influential view linking MNS and ASD (Williams et al.
2001). MNS activity characterizing goals and actions must be bound to other neural systems recognizing agents and
objects – a point that is emphasized in a brief detour into the problem of alien voices and hands in schizophrenia
(Arbib & Mundhenk 2005) – and I will argue that defects in binding of mirror neuron activity may be an important
contributor to some deficits in ASD. I then use an fMRI study of imitation of facial expressions of emotion (Dapretto
et al. 2006) to show that children with ASD can develop compensatory strategies by exploiting different neural
mechanisms to capture some aspects of a socially relevant behavior. I complement discussion of the relevance of
mirror neurons to the analysis of ASD by also considering approaches based on Theory of Mind and briefly discuss
the roles of the amygdala and other brain regions. Finally, I suggest the promise of incremental computer modeling of
“the Mirror System and Beyond.”
Key Words: Mirror Neurons – Autism – Autism Spectrum Disorder (ASD) – Mirror Neuron Systems (MNS) –
Socially Relevant Behavior – Theory Of Mind – Amygdala
Declaration of interest: None
Corresponding Author
Michael A. Arbib
University of Southern California Brain Project
[email protected]
As background we provide a brief characterization
of the spectrum of neurodevelopmental disorders known
as Autistic Spectrum Disorders (ASD), introduce the
notion of mirror neuron system (MNS), and then briefly
summarize a theory relating ASD to deficits in mirror
neurons to set the stage for the rest of the paper.
Some Characteristics of ASD
Children with ASD are not impaired in:
•
Object permanence understanding
•
Tool use
•
Object categorization
•
Attachment
•
Self recognition
but (with differing severity depending on where children
lie on the autism disorder spectrum – which should not
be thought of as one-dimensional) are impaired in:
•
Other recognition
•
Social interaction & Communication/Language
•
Play behavior
•
Imitation & Pantomime
•
Emotion perception
•
Shared attention
•
Pretense
1
This paper is based on a presentation at the Workshop on “Neurocognitive Development and Autism: The Mirror Neuron
Hypothesis” sponsored by Autism Speaks and the National Science Foundation (NSF), and held July 23-24, 2007 at NSF in
Arlington, VA, USA. A preliminary version was circulated on-line for the Awares international online autism conference, November
26-30, 2007, http://www.awares.org/conferences/. The author claims no special expertise in autism (though he did co-author
essays offering [now outdated] analyses linking autism to cybernetic mechanisms many years ago (Arbib & Kahn 1969, Kahn &
Arbib 1973)), but speaks rather from his long-standing involvement in computational cognitive neuroscience, with much attention
to mirror neurons in the last decade or so. My thanks to Justin Williams for his perceptive comments on an earlier draft.
SUBMITTED NOVEMBER 2007, ACCEPTED MARCH 2008
208
© 2007 Giovanni Fioriti Editore s.r.l.
Autism – More than the Mirror System
I cannot address all these topics in the space of a
single article, but hope to provide a useful perspective
on a number of them.
Some Characteristics of MNS
As background for the hypothesis that ASD is
related to impairment of the mirror system in the
developing child, I review relevant data on mirror
neurons. Many neurons in the hand region of ventral
premotor area F5 in macaque monkeys show activity
in correlation with the grasp type being executed
(Rizzolatti et al. 1988). A subpopulation of these
neurons, the mirror neurons (MNs), also respond to the
observation of goal-directed movements performed by
another monkey or an experimenter (e.g. precision pinch
or power grip) for grasps more or less congruent with
those associated with the motor activity of the neuron
(di Pellegrino et al. 1992). By contrast, canonical
neurons in F5 fire when a monkey executes certain
grasps but not when he observes another’s actions. The
same area includes audio-visual mirror neurons (Kohler
et al. 2002) that respond not only to the view but also
to the sound of actions which have typical sounds (e.g.
breaking a peanut, tearing paper). The actions
associated with mirror neurons in the monkey seem to
be transitive, i.e. to involve action upon an object rather
than gesturing “in thin air” and apply even to an object
just recently hidden from view (Umiltà et al. 2001).
Further data address the role of mirror neurons in
the oro-facial area of macaque F5. Ferrari et al. (2003)
showed that about one-third of F5 mouth motor neurons
also discharge when the monkey observes another
individual performing mouth actions. The majority of
these ‘mouth mirror neurons’ become active during the
execution and observation of mouth actions related to
ingestive functions such as grasping, sucking or
breaking food. Another population of mouth mirror
neurons also discharges during the execution of
ingestive actions, but have communicative mouth
gestures (e.g. lip smacking) as their most effective
visual stimuli. Ferrari et al. (2005) find that the
observation and/or hearing of the eating actions of
others facilitate eating behaviors in pig-tailed macaques
and propose that this facilitation of eating rests on the
mirror neuron system of ventral premotor cortex. Coudé
et al. (2007) trained monkeys to vocalize (with a coo
call) for a reward when a piece of food was placed on a
table facing them, and did find some F5 cells that fired
in relation to such vocalization, but no evidence is yet
available for reliable F5 control of normal vocalization
nor of mirror neurons in F5 for such vocalization.
Returning to mirror neurons for grasping, we may
note the following: Perrett et al. (Carey et al. 1997,
Perrett et al. 1990) found that STSa, in the rostral part
of the superior temporal sulcus (STS, itself part of the
temporal lobe), has neurons which discharge when the
monkey observes such biological actions as walking,
turning the head, bending the torso and moving the
arms. Of most relevance to us is that a few of these
neurons discharged when the monkey observed goaldirected hand movements, such as grasping objects
(Perrett et al. 1990) - though STSa neurons do not seem
to discharge during movement execution as distinct
Clinical Neuropsychiatry (2007) 4, 5-6
from observation.
STSa and F5 may be indirectly connected via
inferior parietal area PF (Brodmann area [BA] 7b)
(Cavada & Goldman-Rakic 1989, Matelli et al. 1986,
Seltzer & Pandya 1994). About 40% of the visually
responsive neurons in PF are active for observation of
actions such as holding, placing, reaching, grasping and
bimanual interaction. Moreover, most of these action
observation neurons were also active during the
execution of actions similar to those for which they
were “observers”, and were thus called PF mirror
neurons (Fogassi et al. 1998). In summary, area F5 and
area PF include an observation/execution matching
system: When the monkey observes an action that
resembles one in its movement repertoire, a subset of
the F5 and PF mirror neurons is activated which also
discharge when a similar action is executed by the
monkey itself.
We have only one dataset related to possible mirror
neurons in humans (Mukamel et al. 2007) since single
neuron recording is only possible in very rare cases in
humans, during neurosurgery. Therefore, one usually
talks about a mirror region or a mirror neuron system
(MNS) in humans, identified by brain imaging (PET,
fMRI, MEG, etc.) which is activated relative to a control
task both for observation of a class of actions and for
execution of that class of actions. An increasing number
of human brain mapping studies now refer to “the”
mirror system. However, different brain regions may
be implicated as mirror regions or MNSs for different
classes of actions. Thus it is important to speak of multiple MNSs. Collectively these data indicate that action
observation activates certain regions involved in the
execution of actions (or emotions) of the same class.
Because of the overlapping neural substrate for action
execution and observation in humans as well as other
primates, many researchers have attributed high level
cognitive functions to MNs such as imitation (Carr et
al. 2003), intention attribution (Iacoboni et al. 2005)
and – on the finding of a mirror system for grasping in
or near human Broca’s area – language (Rizzolatti &
Arbib 1998). However, monkeys do not imitate (save
in some simple fashion – see, for example, Visalberghi
& Fragaszy 1990) or learn language and so any account
of the role of mirror neurons in imitation and language
must include an account of the evolution of the human
mirror system (Arbib 2005, Rizzolatti & Arbib 1998)
and related brain regions, as well as the biological
triggers that can unleash in monkeys a rudimentary
imitation capability that goes beyond those they
normally exhibit, though still being quite limited
compared to those of humans (Kumashiro et al. 2002).
Thus imitation and language – and other functions
impaired in ASD – are not inherent in a macaque-like
mirror system but instead may depend on the embedding
of circuitry homologous to that of the macaque in more
extended systems within the human brain.
Consider, for example, the claim that the mirror
system for grasping first evolved to mediate social
understanding. My counter-hypothesis is that:
a: The mirror system for grasping evolved originally
to provide visual feedback for those hand
movements requiring attention to object detail;
b: Exaptation exploited this “self-ability” to map
other individual’s actions into internal motor
209
Michael A. Arbib
representations; and that
Understanding and Planning involve far more than
the mirror systems, as in Figure 1.
We stress the important role of social interaction
in the forming of emotions. Human emotions are greatly
influenced by our ability to empathize with the behavior
of other people. Mirror neurons have been implicated
in empathy – but with the emphasis not only on
recognizing facial expressions but also on empathizing
with the “emotional stance” of other actions. Gazzola
et al. (2006) offer fMRI evidence for an auditory-visual
mirror system in humans comprising a left hemispheric
temporo-parieto-premotor circuit with a dorsal cluster
more involved for hand actions, and a ventral cluster
more involved for mouth actions. Moreover, individuals
who scored higher on the perspective taking component
of an empathy scale activated this system more strongly,
which the authors adduce as evidence for a possible
link between the motor mirror system and empathy.
But note that, since we cannot see our own faces,
a mirror system for facial expression must involve a
different evolutionary scenario than that I have posited
for the mirror system for grasping. This reinforces the
warning that we must not talk of the mirror system but
rather seek to understand the roles of, and interactions
between, multiple mirror systems.
Echopraxia and echolalia are imitation-like
phenomena that are accentuated in autism (Libby et al.
1997, Roberts 1989): Repetitive and stereotyped
behaviors and speech may be copied from others –
words and phrases (echolalia) and sometimes actions
(echopraxia) may be mimicked without regard to their
normal goals and meanings.
What does this tell us about MNSs? First, recall
that monkeys hardly imitate (Visalberghi & Fragaszy
1990) yet have mirror neurons, so that these neurons in
some sense only provide “half” the mechanism for
imitation – having neurons that represent the action of
another does not imply that this representation is “wired
up” to drive the circuitry for execution of that action.
(Caution: Presumably young monkeys are fully social
despite their lack of “complex imitation”. Empirical
c:
Issue: What aspects of human sociality does a fully
social monkey or ape share, what does he lack?)
Figure 2 extends Figure 1 to emphasize the
connection (a) which may provide feedback for selfactions, but in monkeys seems not to provide a path
from recognizing the action of another to repeating that
action. However, even where such a path exists to
support imitation (as in humans but not, presumably,
in monkeys), it is normally under inhibitory control,
since the appropriate response to another’s action is
rarely to repeat it. It is, I suggest, this inhibition that is
impaired in echopraxia and echolalia.
Turning from praxic actions to emotions, consider
emotional contagion (Hatfield et al. 1994, Provine
1997):
1) Since emotional states are closely linked to
certain facial expressions, observation of a facial
expression might result in mirrored (but mainly
inhibited) pre-motor activation in the observer and a
corresponding “retrodicted” emotional state.
2) Such a process might help to explain the
phenomenon of emotional contagion, in which people
automatically mirror the postures and moods of others.
Indeed, the former may be like neonatal imitation
(Meltzoff & Moore 1977) in facilitating the use of
certain effectors or muscle groups rather than capturing
the specific goals and actions of a behavior.
It has been suggested that mirror neurons can
contribute not only to “simulating” other people’s
actions as the basis for imitation, but also ‘simulating’
other people’s feelings as the basis for empathy (Gallese
& Goldman 1998, Goldman 2006, Jacob & Jeannerod
2005). However, this cannot be the whole story. If we
see a photo of a person’s home destroyed by fire or
flood, we empathize with them without seeing their
actions or emotions, so that if our mirror neurons are
activated it cannot be by recognition of the other’s
actions, but rather by, e.g., more general associative
mechanisms linking loss with sadness. Again, if we
recognize anger directed at us by another person, our
response may be to react with anger or fear but in neither
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Figure 1. Understanding and planning involve far more
than the mirror systems
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Figure 2. Inhibiting a direct path from action observation to
action execution to block echopraxia
Clinical Neuropsychiatry (2007) 4, 5-6
Autism – More than the Mirror System
case to empathize with their anger; whereas if their
anger is directed at a third party, then empathy with
their anger is a possible reaction. Note that in any case
we must recognize a binding problem for mirror
neurons. Whether for MNs representing an action or
an emotion, the brain must appropriately bind the
activity of a set of mirror neurons to the appropriate
agent, whether the first person, second person, or one
of multiple third persons.
Given all this, it will be useful to set forth a number
of key points about mirror systems before considering
in more detail their relation to ASD:
i. The “classic” mirror system for grasping is the set
of mirror neurons discovered in macaque F5,
augmented by the related neurons with mirror
properties in PF. STSa provides visual input to PF
but seems not to contain mirror neurons.
ii. Subsequent studies have shown that some of these
neurons also can respond to the sound of actions,
while neurons in the oro-facial zone of F5 have
mirror properties linking ingestive and certain
communicative gestures but not (with a possible
minor exception) vocalizations.
iii. Human brain imaging identifies a “mirror system”
for grasping in human Broca’s area and IPL.
iv. Further brain imaging studies also implicate these
regions in imitation, imagination and language.
v. Caveat 1: Since macaque F5 contains many
neurons that are not mirror neurons, it is a mistake
to conclude that activity in such a region is “mirror
neuron activity”. Moreover, we must note that a
“mirror system” need not contain mirror neurons!
All that is required is that it contain both neurons
active for action execution and neurons active for
action observation.
vi. Caveat 2: The activity of mirror neurons rests on
the activity of many other brain regions. Thus it is
mistaken to think that mirror neurons per se can
account for imitation, imagination and language
– especially since monkeys have little skill in
imitation and no use of language (as distinct from
a system of innate calls).
vii. We nonetheless consider that the human
homologues of the F5 and related parietal mirror
system have mirror neurons not only for limb
movements but also facial expressions and
communicative gestures. When we speak of “the
mirror system hypothesis of autism”, we refer to
the impact of deficiencies in these “core” mirror
systems.
viii. However, there is no reason to think that these core
systems are the only places in the human brain
where imaging will yield activation both for “doing
something” and for “observing someone else doing
it”. Thus, Cattaneo et al. (2007) assert that, in
humans, the mirror neuron system has two major
components. One is formed by the inferior parietal
lobule and the ventral premotor cortex plus the
caudal part of Broca’s area (i.e., the system we
have just described) and the other by the insula
and anterior cingulate gyrus. Besides its originally
proposed role in action understanding, the parieto–
frontal system appears to mediate the
understanding of intentions of others and imitation,
whereas the insular–cingulate system appears to
Clinical Neuropsychiatry (2007) 4, 5-6
play a fundamental role in emotion recognition
(Gallese et al. 2004, Singer et al. 2004). However,
(a) the parieto–frontal system may be involved in
understanding of intentions of others and imitation,
but only as part of a larger neural system, and (b)
the insular-cingulate system is not a mirror system
in the sense defined above.
ix. Thus, to the extent that we seek to find genetic
correlates for autism, we can expect different
symptom-complexes to be associated with (a)
genetic changes that affect the parieto–frontal
system and (b) genetic changes that affect the
insular–cingulate system, whether or not the latter
should be considered as a mirror system. Thus, in
this paper, when I talk of “multiple mirror systems”
I will be focusing on the various components of
the “core” parieto–frontal system, and will continue to stress that these components function
effectively only through their connections with
other brain regions – connections which differ
greatly between macaque and human.
x. In particular, then, when discussion of ASD
symptoms turns to agency attribution, “theory of
mind” and empathy, I am not postulating additional
mirror systems but rather asking to what extent
these functions depend on core mirror systems
within the action-processing framework, and to
what extent they depend on other brain
mechanisms.
Linking MNSs and ASD
Williams et al. (2001) suggested that a failure in
the development of the mirror neuron system is behind
autism and that, moreover, in autism the mirror neuron
system is malfunctioning as a whole. They hypothesize
that early developmental failures of mirror neuron
systems lead to a cascade of developmental impairments
that accumulate to yield the clinical syndrome of autism.
They focus on a disturbance involving difficulties both
in imitating actions and in inhibiting more stereotyped
mimicking. To the latter point, consider the repetitive,
inflexible and stereotyped behavior and language – the
echopraxia and echolalia mentioned previously – that
appears to incorporate some copying from others, in
some patients with autism. I suggested (Figure 2) that
a controlled inhibitory system is essential for allowing
MN’s to operate “off-line”. If damage extends to such
inhibitory components, Williams et al. (2001) suggest
that certain forms of mimicry might occur, yet be oddly
performed. This may be too simple. Loss of inhibition
still leaves the MNS functioning. It does not account
for the dissociation of imitation and echopraxic
mimicry. Moreover, the understanding of others’
intentions by children with ASD is largely intact
(Carpenter et al. 2001).
Williams et al. (2001) further argue that mirror
neurons may be key elements facilitating the early
imitation of actions, the development of language,
executive function and the many components of ToM
(Theory of Mind, about which more below). They concede that the heterogeneity of ASD may argue against
a single cause, yet suggest that the commonalities of
the clinical syndrome nevertheless permit the possibility
211
Michael A. Arbib
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Figure 3. The dual route model of praxis (the middle and right columns, echoing the language system on the left) in which an
action may be imitated via the indirect route in which mirror neurons (in the input praxicon) activate known motor schemas
(the output praxicon) or via the direct route in which the action is imitated as an assemblage of meaningless gestures (Adapted
from Rothi et al. 1991)
of a core dysfunctional mechanism. My counter-point
will be that we must go Beyond the Mirror to understand
the wide plexus of systems linked to but going beyond,
the basic F5/Broca’s area mirror neurons.2 We must also
address the question of whether an MNS translate
between selves, or simply “ignores” the self. I later
discuss the work of Arbib and Mundhenk (2005)
concerning the extra machinery that may be required
to link an action to a self – whether oneself or another.
To proceed further, it will be useful to consider a
conceptual model that addresses data on apraxia.
Addressing the observation that some apraxic patients
are unable to pantomime common actions or imitate
meaningful gestures but are nonetheless able to imitate
meaningless gestures, Rothi, Ochipa, and Heilman
(1991) offered the dual route imitation learning model
balancing language and praxis which is adapted in Figure 3, where I indicate that the right-hand (praxis) side
should be augmented by an action buffer. The input
praxicon corresponds to recognition of a familiar action
(and is thus part of a mirror system), which can then be
“imitated” by using an existing motor schema in the
output praxicon to re-create the action. (The
terminology is defined by analogy: the praxicon is for
praxis [practical action] what the lexicon is for
language). By contrast, the direct route, it is claimed,
does not involve re-creation of the action as a whole
(which includes activation of the semantics of the
action) but rather involves piecemeal analysis of the
observed action which allows it to be re-created as a
“semantics-free” assemblage of motor features.
However, where Rothi et al. (1991) distinguish a
direct and indirect route based on a dissociation between
the ability to pantomime a meaningful action and the
ability to imitate a meaningless gesture, I would argue
that this mistakes the primary role of the direct route –
we did not evolve to make meaningless gestures.
Instead, I hypothesize that our evolving skill in imitation
rested in part on the ability not only to acquire novel
actions through blind trial-and-error and through the
assemblage of known actions, but in addition that the
direct route evolved so that familiar tweaks (small intransitive movements that are frequent components of
many actions) could be used to adjust a known action
to better match an observed novel action. Only later
was the direct route exapted for novel gesture imitation.
An action combines a motion and a goal and,
recognizing the goal, we may fail to pay attention to
the details of the motion that achieves it. Whatever the
fate of this hypothesis, the key point is that the direct
route is, in evolutionary terms, more sophisticated than
the indirect route and that the passage from the common
ancestor of monkeys and humans to humans involves
the ability to dissociate (some) motions from explicit
goals. When engaged in stereotypic behavior, the child
with ASD seems to focus on the motion without
2
Williams (2008, to appear) offers a more nuanced view, based on recent data, which continues to emphasize the role of
mirror neurons, but also notes the importance of the amygdala and orbitofrontal cortex, among other brain regions. However,
my emphasis in the present section is on the ideas of the 2001 paper. For an alternative approach to linking mirror neurons and
autism, inspired in part by EEG data on µ-waves (Oberman et al. 2005), see Ramachandran & Oberman (2006) and Oberman
& Ramachandran (2007).
212
Clinical Neuropsychiatry (2007) 4, 5-6
Autism – More than the Mirror System
reference to achieving some associated goal. Thus s/he
may not so much be “reverting” to the ancestral system
as holding on to one new capability (dissociating the
motion from the goal) while losing the complementary
ability to infer the goal from the motion.
However, we need to look in more detail at the
following data: Imitation of meaningless gestures is
affected more than imitation of actions with objects
(Rogers et al. 1996). Children with autism were more
likely to make errors when asked to imitate an
unconventional action with a common object (such as
drinking from a teapot). Perhaps the use of appropriate
objects helps to shape a matching response; by contrast,
difficulties in copying raw gestures underlines the more
basic nature of the imitative deficit referred to earlier
(Merians et al. 1997). This may suggest that the deficit
is not at the ancestral level (i.e., at the level of mirror
system mechanisms we share with nonhuman primates),
but in the “higher” extensions. There are greater group
differences with respect to sequences of actions than
when single actions alone are being imitated, suggesting
that we need to look beyond mirror systems in isolation
to their linkage in sequential action with the basal
ganglia and prefrontal cortex (Ring & Serra-Mestres
2002). Patients with ASD have evident imitation deficits
(Pennington & Bennetto 1998). Mechanisms underlying
imitation could be precursors to full ToM (Rogers &
Pennington 1991). Imitation does not require ToM,
since it can proceed on the basis of overt behavior
without ascription of intentions to the imitatee. Imitation
may also be fundamental to the other, broader kinds of
social deficits seen in autism, but this does not address
repetitive and stereotyped behavior.
Rogers and Pennington (1991) talk of the
“impaired formation/co-ordination of specific self-other
representations” as being at the root of the cascade of
problems of children with ASD. This in turn could
explain the failure to develop reciprocal social abilities
including shared/joint attention, gestural recognition
and language (particularly the social/pragmatic aspects
that Rogers and Pennington (1991) note are the most
affected), as well as breakdowns in the development of
empathy and a full ToM.
However, to fully appreciate the implications of
such observations we must distinguish what a mirror
systems does from the roles of other regions to which
it is linked. Returning to the MNS for grasping, I stress
that the activity of an F5 mirror neuron for a particular
type of grasp (say, Grasp-A) is only part of the code for
Grasp-A(Agent, Object), specifying which Agent
grasps which object. The full neural representation of
the “Cognitive Form” (CF): Grasp-A(Agent, Object)
further requires inferotemporal cortex which holds the
identity of the object and regions of the brain, such as
those involved in face recognition, which hold the
identity of the agent. How these representations are
bound together remains a research challenge. But the
implications for autism may be better understood by a
brief detour into the study of schizophrenia.
Schizophrenia: Alien Voices and Hands
I briefly summarize an essay (Arbib & Mundhenk
2005) inspired by data on schizophrenic subjects (see
Clinical Neuropsychiatry (2007) 4, 5-6
Arbib 2007 for related observations) concerning:
· auditory verbal hallucinations (AVH): the
subject may believe he is 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 he reports hearing.
· Delusions of influence: The arm of the patient
may move, but the patient attributes it to an external
influence.
The essay responded particularly to a study by
Daprati et al. (1997, and see Franck et al. 2001 for
related data) of so-called agency, i.e., in knowing who
was the agent of a particular action. 30 normal control
subjects and 30 schizophrenic patients performed a
requested movement with the right hand, and monitored
its execution by looking at 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 in any other case, that is if you
doubt that it was your own hand or your own
movement.”
In each trial the subject was presented with an
image 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 seeing 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 in the control group, 17 in
the non-delusional group and 23 in the delusional group.
Daprati et al. (1997) suggest these show a problem for
schizophrenics in their sense of agency, but Arbib and
Mundhenk (2005) counter that the experiment has
nothing to do with attribution of agency: In each case,
it seems that the subject knows that he has himself 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. They
thus argue that two different factors may affect the
symptoms of schizophrenia of concern here, selfmonitoring and attribution of agency:
Self-Monitoring: Did I knock over that glass when
I swept my arm backward?
Agency Attribution: I see/hear hammering? Who
is doing it?
We rarely recognize the agent from a hand
movement alone. We must connect the hand to a
recognizable person – e.g., by linking the hand to a
recognizable face, walk, voice, style of clothing, etc.
We can then distinguish two levels of attributing an
action:
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. Lack of knowledge introduces the risk
of confabulation.
Arbib and Mundhenk (2005) argue that in general
the brain simply processes self-actions without need to
213
Michael A. Arbib
attribute agency to the action – the brain simply does
its job of integrating perception, plan and action.
However, if one’s hand moves in an unexpected way,
one may ask “What made my arm hand that way?” and
the answer might be “I was moving it intentionally but
…” or “I did not intend to move it, but …”. In other
words, the unexpected outcome invokes two processes:
Agency Attribution: In general, the world may
present many alternative actions for our (conscious or
unconscious) consideration. Thus there may be priming
of multiple actions, with tonic inhibition preventing the
execution of any of them. However, cortical processes
interacting with the basal ganglia can disinhibit one of
these actions leading to execution of the action.
(Normally, the basal ganglia inhibit a set of candidate
next-actions until instructed to “release” one of them;
see Dominey & Arbib (1992, Dominey et al. 1995) for
a computational model of such disinhibition for the case
of saccadic eye movements.) Such cortically instructed
disinhibition is, on this account, a reliable neural
correlate of an intended action. However, if the tonic
inhibition from the basal ganglia were weakened, then
some actions could “slip through” without in this sense
being intended.
Self-Monitoring: Arbib and Mundhenk (2005)
further hypothesize that each intended action is
accompanied by a more or less accurate motor working
memory of the trajectory of the action.
Thus if the need arises to question the agency of
the action, the brain may consult its working memories
to see whether the observed movement matches the
working memory of an intended movement and if so
whether the working memory of the expected outcome
of the action sufficiently matches the observed
trajectory of the outcome. On this basis, the normal
brain can decide “I am the agent”, “I was the agent but
for some reason the action did not come out as
intended”, or “I am not the agent”.
The same hypothesis accounts for auditory verbal
hallucinations. Schizophrenic patients hallucinate
voices that they attribute to external agents; they also
have delusions that other people are creating their
actions for them and also of influencing others to act
(DSM-IV 1994). In addition, patients with
schizophrenia have difficulty determining whether they
spoke or thought an utterance (Brébion et al. 2002,
Franck et al. 2000). Given this, Mundhenk & I suggest
that the primary deficit here is in the lack of adequate
control of disinhibition so that an action may be
committed without there being a disinhibitory signal
that represents the decision to execute the action.
Lacking any memory of having intended the action,
the patient concludes “I am not the agent” and then
proceeds to confabulate, to provide an account for the
agency of the observed action. This account is consistent
with – but offers a fresh perspective on – the hypothesis
that the problems of schizophrenia involve working
memory (Perlstein et al. 2003, Posada et al. 2001).
An intriguing research challenge, then, is to
understand what distinguishes the lack of inhibition that
yields auditory verbal hallucinations and delusions of
influence in the schizophrenic from the lack of
inhibition that yields echopraxia and echolalia in those
children with ASD who exhibit it. My preliminary
suggestion is to posit in schizophrenics a deficit in the
214
inhibition which controls which one among alternative
courses of action will be executed, while in echopraxia
and echolalia the deficit is in the inhibition of the path
from action observation to action execution shown in
Figure 2.
A Challenge for Understanding and Intervention
We now recall an fMRI study (Dapretto et al. 2006)
linking increased severity of ASD to reduced activity
in “the mirror system”. Stimuli consisted of 80 faces
expressing five different emotions: anger, fear,
happiness, neutrality or sadness. Subjects either imitated
or simply observed the faces. Brain activity (the BOLD
signal of fMRI) was studied during imitation of
emotional expressions by (a) a typically developing
group; and (b) an ASD group. Activity in bilateral pars
opercularis of the inferior frontal gyrus – often
identified as the site of the frontal range of the human
mirror system – is seen (stronger in the right
hemisphere) in the typically developing group (a) but,
it is asserted, not in the ASD group (b). However, they
found a large left hemisphere overlap for activation of
this region in the 2 groups (Figure 1 of Dapretto et al.
2006). Moreover, lesion and imaging studies have
implicated pars opercularis in a variety of functions in
addition to serving as a mirror system. This raises the
research question: What can be added about precise
localization of relatively greater activation in normals
compared to ASD and, given this, are these “difference
areas” establishable as parts of a mirror system on other
grounds?
Dapretto et al. (2006) indexed symptom severity
in ASD. Controlling for IQ, they found reliable negative correlations between activity in the pars
opercularis and the children’s scores on the social
subscales of the Autism Diagnostic Observation
Schedule–Generic and Autism Diagnostic Observation
Interview–Revised (Lord et al. 2000, Lord et al. 1994)
(see Figure 3 of Dapretto et al. 2006). They conclude
that “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.” However, we
still have the question whether this correlation applies
specifically to the MNS.
Dapretto et al. (2006) not only conducted brain
imaging studies inside the scanner, but also had half
the children in each group perform both tasks during a
videotaped session with an eye tracker. Intriguingly,
there were no group differences in the amount of time
spent fixating on the face and eye region, nor in how
well the children imitated facial expressions. This raises
a Disturbing Thought: Perhaps an MNS is not important
for recognition of facial expressions! However,
returning to fMRI data, children with ASD showed
greater activity than did the typically developing
children in right visual and left anterior parietal areas
which are regions known 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 are quite
different. Such findings suggest the relevance of the
Clinical Neuropsychiatry (2007) 4, 5-6
Autism – More than the Mirror System
following comments by (Rutter 2005):
… children [with ASD] 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. … [Research] … has
concentrated on the deficits rather than on the equally
important question of the compensatory cognitive
strategies that individuals with autism use.
The study by Dapretto et al. (2006) combines with
these comments to suggest that – no matter what future
research reveals about the neural correlates of autism –
the search for alternative strategies for reaching
functional goals will continue to be of great importance.
Indeed, the “two route solution” for facial imitation has
echoes of the discussion of direct versus indirect routes
for imitation in the study of apraxia (recall Figure 3
above). In the present example, I distinguish (i) the “gut
semantics” of emotion which links activation in, e.g.,
amygdala, orbitofrontal cortex and insula to the
embodiment (somatic/visceral) of emotions and the
attendant “feelings” from (ii) the “disposition
semantics” of recognizing that a certain facial
expression may betoken a behavioral disposition but
without feeling the attendant emotion. This suggests
that the subject with ASD might lack that part of the
mirror system that links an “indirect route” to “gut
semantics”, and yet be able to exploit a direct route
that can build representations of facial expressions
which lack this direct linkage to emotional feeling. The
latter representations may still become paired with
behavioral disposition through a process of associative
learning. It is worth noting that this still requires a mirror
system, but it is a mirror system divorced from those
neural regions which yield emotional feelings.
Theory of Mind
Leslie (1987) distinguished two types of representation when analyzing the cognitive mechanism
underlying shared attention and pretense:
First-order representations describe visible bodies
and events.
Second-order representations describe invisible
minds and mental events and serve to make sense of
otherwise contradictory or incongruous information.
These constitute a person’s Theory of Mind (ToM). The
crucial point about ToM is not only that the child comes
to appreciate “I am like the other/The other is like me”
even for states that are not necessarily visible externally,
but also to understand that the self and the other may
differ in the states they are experiencing.3
A standard test of whether a child understands that
different people may have different mental states is the
Sally-Anne task. The subject is shown a series of
pictures in which: (i) Anne sees Sally place a ball in a
basket and cover it. (ii) Sally leaves the room. (iii) Anne
moves the ball to a box and closes it, replacing the cover
on the basket. (iv) Sally returns. The subject is asked:
“Where will Sally look for the ball after she returns to
the room?” The 2 or 3 year old, and the older child
with ASD, says “In the box” (Baron-Cohen et al. 1985,
see C. D. Frith & Frith 1999 for possible neural
correlates). The older normal child “who has Theory
of Mind” says “In the basket”. Note that the crucial
change here is not in having a generic theory of mind
but rather in understanding that different people can
know different things and understand that Sally’s mind
is still “in the old state” even though the subject has
seen the ball moved and knows that it is in the box.
Consider, for contrast, the photograph task. Here
the child sees a series of pictures showing (i) a bed, a
chair and a bear on the chair; (ii) a camera taking a
photograph of the scene with the photograph being
removed from the camera; and (iii) the bear being
moved to the bed. Intriguingly, even the child with ASD
has ToP (Theory of Photography!) – they know that the
photograph will still show the bear in the chair even
though the bear is now on the bed. This reinforces the
point that there is no one grand ToM but rather a
growing set of special skills (and some generalizations)
about other people which can be present or absent in
diverse combinations.
Another way to address the issue of “adopting
another’s perspective” is to use 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, unlike
normally developing children, will try to imitate the
scene by facing the palms of their hands to themselves,
instead of to the person who was making the test, i.e.,
they reproduce the effect the action had on them, rather
than the original action as performed by its agent. This
makes the point that both imitation and attribution of
mental states involve translating from the perspective
of another individual to oneself. Such considerations
have led to the hypothesis (Carruthers & Smith 1996,
Whiten 1996) that the beliefs of children with ASD are
based solely on their first-order perceptions of the
world.
But a niggling doubt remains: It’s not just
perspective. The Polaroid photograph task shows that
the child with ASD can change perspective. Of course,
it can be objected that a photograph is “first-order” even
if it is still inside the camera. But recall the definitions:
First-order representations describe visible bodies
and events.
Second-order representations describe invisible
minds and mental events.
This omits what I will call indirect representations
which describe “invisible” events, and in particular refer
to internal states of objects and actors which affect one’s
predictions about them. Mental events (second-order
representations in the above sense) are then a special
case of indirect representations. The crucial point of
the Polaroid photograph task is that the child with ASD
3
The present section builds in part on the discussion of Theory of Mind in Williams et al. (2001). I would prefer (a lost
battle) to use the term Models of Other Minds (MoOM) to stress that what is vital is not a “theory of mental behavior” but
rather an understanding of the mental states and dispositions of others as they vary from occasion to occasion.
Clinical Neuropsychiatry (2007) 4, 5-6
215
Michael A. Arbib
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 …” Again, I suggest that we view ToM as a
collection of diverse skills. This discussion links back
to my presentation of the Dapretto et al. (2006) finding
that ASD children could successfully imitate facial
expressions, but using different neural strategies from
those adopted by typically developing children; and the
observation (Rutter 2005) that research “has
concentrated on the deficits rather than on the equally
important question of the compensatory cognitive
strategies that individuals with autism use.” What I am
suggesting is that training of ASD children in the use
of indirect representations in relating facial expressions
to behavioral dispositions may yield most of the benefits
that typically developing children may gain from a more
integrated appreciation of how the mental states of
others relate to, yet differ from, their own
Baron-Cohen, Leslie, and Frith (1985) argued that
difficulties of children with ASD 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, while 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., that the primary deficit is socio-affective, a
lack of empathic and emotional engagement with
others. However, given the great range of symptoms
across the autistic spectrum, talk of the primary deficit
seems misleading at best. Indeed, some problems in
ASD appear ill accommodated by a primary ToM or
socio-affective deficit. These include repetitive and
stereotyped behavior (including copied behaviors),
obsessive desire for sameness, delayed and deviant
language development (including echolalia), and
difficulties in perceiving or planning at high-levels of
organization (“executive function”).
Meltzoff and Gopnik (1993) proposed that
neonatal imitation could provide a key starting-state
for the development of ToM. Their claim is that the
new-born’s capacity to translate between the seen
behavior of others and what it is like to perform that
same behavior offers a crucial basis for recognizing
the linkage between mental states and actions. However,
we need to distinguish “neonatal” imitation from “real”
imitation. The neonate is “mastering the correspondence
problem” of matching parts of its own body (whether
seen or unseen) to moving parts of other bodies, not
learning about the “feel” of specific behaviors. The
former is more like effector matching and “contagion”
in yawning or smiling. However, neonatal imitation may
build the substrate for “real” imitation. Visual
preshaping for goal-directed manual actions seems
inoperative until about 9 months of age, and it seems
plausible to infer that mirror neurons, and their role in
imitation of novel actions, cannot be in place any earlier
than this (Oztop et al. 2004).
Individuals with ASD experience difficulties in
executive functions (Hughes et al. 1994, Ozonoff &
216
Jensen 1999, Ozonoff et al. 1991) such as planning
ability and attentional shifting. Normal executive
functions may be the product of the individual’s trial
and error, but it is also possible that the child learns
something of these functions from others, perhaps
initially in relatively concrete contexts, such as playing
with building blocks in infancy, and then at higher levels
of abstraction and over longer time frames (ZukowGoldring & Arbib 2007). The initial stages in such a
process might correspond to some kind of “programlevel” imitation of the type involved in apes acquiring
new skills over months of observation of others (Byrne
2003, Byrne & Russon 1998). Griffith et al. (1999)
found that apart from tests requiring rule reversal, there
was no deficit of executive function in children under
4 years of age with autism. (Indeed, whether children
with autism make more reversal errors than properly
matched controls remains unclear; see Williams et al.
2004.) This suggests that the types of executive function
exhibited by normal children younger than four do not
require the proper functioning of processes impaired
by those developmental processes (whose nature still
eludes us) that are impaired in autism. Consider the
similar time-scale for success on the Sally-Anne task.
Some executive functions, including inhibition and
possibly visual working memory appear to be spared
in autism (Hughes 1996, Ozonoff & Strayer 1997,
Russell 1997) though it is unclear how claims for
sparing of inhibition are to be reconciled with the
disinhibition characteristic of echopraxia and echolalia
seen in some children with ASD.
Implicit in the above is a call for a much less
accepting view of the notion of “mental state” as a
unitary concept. The appropriate critique would also
build on my earlier brief analysis of the simulation
theory of empathy (Gallese & Goldman 1998, Goldman
2006, Jacob & Jeannerod 2005). Some authors have
proposed the “Simulation Theory of ToM” which
proposes that children come to read minds by “putting
themselves in the other’s shoes”, and using their own
minds to simulate the mental processes that are likely
to be operating in the other. As noted earlier, a key point
here is to appreciate that the other is “other” – i.e., that
the “simulation” must use different “variables” from
those that describe one’s self. I stated this as the binding
problem for mirror neurons: For mirror neurons for
emotions to function properly in social interaction, not
only must the brain have mirror neurons simultaneously
active for multiple emotions, but it must also bind the
encoding of each emotion (whether self or other) to the
agent who is, or appears to be, experiencing it. I
hypothesize that a mirror neuron system that cannot
solve this binding problem, distinguishing the mental
states of different people, would both yield a number
of autistic symptoms and also show much less activity
in a variety of tasks.
Further Neural Correlates
Children with ASD show not only characteristic
ToM, but also impairment in reconstructing non-routine
events from the personal past and in planning for the
future. Suddendorf and Corballis (1997) proposed that
the executive capacity to disengage or dissociate from
Clinical Neuropsychiatry (2007) 4, 5-6
Autism – More than the Mirror System
one’s actual current state (putting it offline) in order to
simulate alternative states underlies both “theory of
mind” and mental “time-travel” – the ability to mentally
construct possible (e.g. planned) events in the future
and reconstruct personal events from the past. Thus, in
this account mirror neurons may be involved through
simulation and executive functions. However, this also
looks “beyond the mirror”, e.g., access to the personal
past might involve linking MNSs with hippocampus ,
whereas future planning could involve linking MNS
with prefrontal cortex. In either case, we see another
version of the binding problem for mirror neurons –
though here the binding must distinguish “self-now”
from “self-then” or “self-hypothetical” rather than
“self” versus “other”.
Frith & Frith (2000) reviewed brain imaging
studies of both typical individuals and those with
autism, seeking to identify sites active in ToM functions.
They found that a well demarcated area of the
paracingulate gyrus has been consistently implicated,
as have areas of the anterior cingulate cortex – but not
the mirror neuron regions. The paracingulate gyrus and
the anterior cingulate cortex are closely linked and
receive dense serotonergic innervation. One possible
reason for the failure of these tasks to activate MN
regions may be related to the control tasks that have
been used or we may have the type of distinction
between “basic emotions” and “declarative emotions”
that came up in my linkage of the Dapretto et al. (2006)
results to the dual route notions of Rothi et al. (1991).
Other MRI studies have revealed abnormalities in
subcortical regions, particularly in the cerebellum where
a reduced vermis and Purkinje cells were found in its
posterior and inferior areas. Riva and Giorgi (2000)
found that cerebellar vermal lesions led to two profiles:
(i) post-surgical mutism, which evolved into speech
disorders or language disturbances similar to
agrammatism; and (ii) behavioral disturbances ranging
from irritability to behaviors reminiscent of autism. In
addition, cerebellar and hippocampal changes have been
related to symptoms of autism (Bauman & Kemper
2005). Cerebellar damage could produce lack of gaze
control (needed for joint attention) and lack of response
reassignment (needed for multiple goal directed
activities such as social interactions). Hippocampal
lesions impair precise representation of temporal
information across a range of tasks and would impair
construction of a time-space map of events. Such
mapping is vital for extracting abstract structure from
sequences of events to produce second-order
representations.
Baron-Cohen et al. (2000) found altered functioning in different brain regions including the medial
prefrontal cortex and the amygdala. They advocated
“the amygdala theory of autism”: In an fMRI study
involving judging from the expressions of another
person’s eyes what that other person might be thinking
or feeling, patients with autism did not activate the
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Figure 4. Salvador Mármol’s schematic of the “Beyond the Mirror System” highlighting functions and interactions whose
impairment may be implicated in various aspects of Autistic Spectrum Disorders (Mármol Yahya 2002, unpublished)
Clinical Neuropsychiatry (2007) 4, 5-6
217
Michael A. Arbib
amygdala, whilst people without autism did show
amygdala activity. The amygdala was therefore
proposed to be one of several neural regions that are
abnormal in autism. However, Amaral et al. (2003)
answered negatively the question “Is the amygdala 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. Neonatal animals with
amygdala lesions at 2 weeks of age also demonstrate
species-typical social behaviors such as the generation
of facial expressions as well as grooming and play
behavior. They conclude that the amygdala is not
essential for the interpretation of social communication
or for the expression of social behavior. Amygdala does
appear to participate in the evaluation of the “safety”
of social interactions and so, they suggest, may have a
role in modulating the amount of social behavior in
which an organism will participate.
Such considerations led Salvador Mármol to
develop the scheme shown in Figure 4 (Mármol Yahya
2002, unpublished). The point here is not to debate the
adequacy of this scheme (though thought-provoking,
it is surely too simple) but rather to indicate the
challenges of charting the manifold interactions of the
brain wherein a variety of different malfunctions can
conspire to place a child on the road to ASD.
Modeling the Mirror System and Beyond
It is well understood that ASD is linked to changes
in many genes, and increasingly well understood that
across the spectrum of ASD we see differential changes
in many brain regions. Much data from molecular
biology and brain imaging, etc., will be required to
characterize these changes. But how do changes within
any one region affect its development and function, and
how does change in one region affect the competition
and cooperation of the larger network of brain regions
of which it is part? My claim is that mere verbal analysis
is inadequate for the long-term challenge, and that only
increasingly complex simulations will be able to chart
this unfolding complexity. I am not unbiased in this
judgment – my primary research is in computational
neuroscience, trying to understand how behavior is
mediated by interaction between various brain regions,
each analyzed in terms of the activity of large neural
circuits (see Arbib 2003a for a non-technical
introduction, and Arbib 2003b for all the gory details),
but I have avoided this type of formal analysis in the
body of the paper. In this Section, I say just enough
about a few models to indicate what is involved.
Figure 5 shows the MNS Model of the Mirror
System for grasping (Oztop & Arbib 2002). It relies on
two visual analyses: one extracts the affordances
(opportunities for grasping) of the attended object; the
other analyzes the motion of the hand and changes of
hand shape. Together, these represent how the hand
approaches the object’s affordances, coding within the
brain hand-object relations in an object-centered coordinate framework. The model shows how synaptic
plasticity can enable a set of trajectories (movement
and preshaping of the hand in relation to an object’s
Figure 5. The MNS Model of the Mirror System Model for grasping (Oztop & Arbib 2002). Note that it involves not only the
mirror system itself, but visual systems along with non-mirror regions of premotor cortex as well as temporal and parietal
cortex. The point is that, to understand even the most basic aspects of the mirror system, one must understand how it is
embedded in, and gains its functionality from, a much larger network of brain regions
218
Clinical Neuropsychiatry (2007) 4, 5-6
Autism – More than the Mirror System
affordances for grasping) to become associated with
the activity of specific sets of mirror neurons. MNS
simulation results show that (a) the model can indeed
appropriately associate sets of trajectories with
classifications of actions (mirror neuron coding); and
(b) the confidence level of these judgments is reduced
by changes in parametric properties of the trajectories.
The moral of this effort is that modeling using adaptive
neural networks supports the view that the repertoire
of the mirror system is acquired rather than innate.
Recent work has developed a more extensive
model of the mirror system for grasping, the MNS2
model (Bonaiuto et al. 2007). It adds two important
capabilities:
1) Audible Grasps: Kohler et al. (2002) found F5
mirror neurons that responded to the sight and sound
of actions with characteristic sounds – such as paper
tearing and nut cracking. MNS2 addresses this by
adding audio input connected to the output layer of the
learning network, with the connections modified with
Hebbian learning. This explains how the mirror system
can learn to pair each grasp type with a different pattern
in the audio input layer if indeed the action has a
distinctive sound pattern.
2) Hidden Grasps: Umiltà et al. (2001) found that
grasp-related mirror neurons will respond to grasps
obscured by a screen as long as an appropriate object
was previously seen before being obscured by a screen.
MNS2 addresses this by adding working memory for
parietal cortex for object and hand information, with
dynamic remapping to update working memory
representation of hand location based on visible arm
movement, mechanisms already explored in early
modeling of the saccadic system (Dominey & Arbib
1992).
My point is not to provide a comprehensive
exposition of the models here, but rather to show that
once one works through in computational detail the
representations and interactions involved in even the
basic workings of the mirror system, one is forced to
consider subtleties that become obscured in a purely
verbal analysis based on the lumping of all the detailed
workings of neural circuitry into a few blobs on an fMRI
scan.
Looking to future work in computational
neuroscience that extends the scheme shown in Figure
5, I note the need for a range of extensions in modeling
the mirror system “and beyond”:
•
Selective attention (attending to the instrument and
object related within the action)
•
Recognizing the object
•
Recognizing the agent
•
The binding problem when actions and emotions
must be bound to different agents
•
Understanding the role of mirror systems and
inhibition in imitation
•
Beyond the hand – what are the commonalities
and differences of mirror systems for hand, face,
articulators, and other effectors?
•
Broadening the linkage to motivational systems
•
Going beyond recognition of single actions to
recognition of sequences and hierarchical actions
•
Integrating the study of transitive and intransitive
actions
•
Language – the Mirror System Hypotheses: (Arbib
Clinical Neuropsychiatry (2007) 4, 5-6
2005, Rizzolatti & Arbib 1998)
And even this menu does not go far enough since
it omits the role of many other brain regions discussed
in the Section on “Further Neural Correlates”.
Manifesto
Let’s stop talking about the mirror neuron system.
Let’s accept that mirror neurons do not
“understand” and try to define their role within larger
systems supporting actual behavior in real life
situations. In particular, more attention is needed to the
fact that a mirror neuron system that cannot solve the
binding problem, distinguishing the mental states of
different people, would yield a number of autistic
symptoms and show much less activity in a variety of
tasks. Other relevant mechanisms whose deficits may
correlate with ASD symptoms include inhibitory
mechanisms, and distinct paths for imitation suggested
by the direct and indirect routes of the praxis model of
Rothi et al. (1991). Detailed analysis of how mirror
systems function within a broader context will help
assess what possibly different MNS defects contribute
to:
•
social deficits
•
communication abnormalities
•
repetitive/stereotyped behavior
while doing justice to important correlates, such
as those on amygdala and orbitofrontal cortex, of other
brain regions with varied symptoms of ASD.
Deeper understanding of mirror systems will rest
not only in brain imaging of humans undergoing a range
of cognitive and other tasks, but also on further research
on monkeys:
•
neurophysiological: more details on, e.g., mirror
neuron outflow;
•
behavioral: Comparing monkey sociality with
normal and autistic human sociality; and
•
comparative/evolutionary: Assessing what
monkeys & humans do/do not share in terms of
imitation, empathy, communication and sociality.
This will ground what we can learn about human
brain mechanisms from such comparisons.
The data and the models reviewed in this article
caution us (i) to avoid viewing the mirror system as
“just a bunch of mirror neurons lighting up for specific
observed actions” and instead look in more detail at
what it takes for mirror neurons to “do their jobs”, and
(ii) to understand that they cannot do these jobs save as
part of larger neural systems “beyond the mirror
system”. I would thus add to the manifesto that
Incremental Computer Modeling should address larger
and larger systems coupled with detailed data on
individual performance (normal and ASD) to test them.
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