Download The role of the mirror neuron system in action understanding and

The role of the mirror neuron system in action understanding and empathy
Bachelor thesis Cognitive Neuroscience
Bachelor program Psychology and Health
Department of Psychology
Dirk van Duijnhoven
ANR: 985752
March 2010
Supervisor: Bernard Stienen
Summary
Mirror neurons have been linked to action understanding in monkeys and humans. It
has even been linked with empathy in humans. This review focuses on the literature
on mirror neurons and the function of these neurons. First of all, the discovery of
mirror neurons in Macaque monkeys and the possibility of the existence of mirror
neurons in humans are described. Subsequently, the role of the mirror neurons in
action understanding and in empathy is discussed. Based on the evidence that actions
can be understood without the mirror neuron system, this paper concludes that it
seems unlikely that the mirror neuron system is the underlying system for action
understanding in monkeys and humans. Hence, it is also not likely that the mirror
neuron system is the underlying system for empathy in humans. Mirror neurons could
be formed through experience as a byproduct of associative learning. However, it
cannot be excluded that the mirror neurons do enrich the experience of observing an
action or emotion.
Keywords: Mirror neurons, action understanding, empathy, mirror neuron system.
Contents
§1 Introduction
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§2 Mirror Neurons in Macaque Monkeys
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§2.1 Properties of the Mirror Neurons
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§2.2 The Mirror Neuron System
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§2.3 The role of the Mirror Neuron System in the Macaque Monkey
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§3 Mirror Neurons in Humans
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§3.1 Mirror Neurons in Humans
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§3.2 Similarities and Differences between the Human and Macaque
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Monkey’s Mirror Neuron System
§4 Action Understanding and the Mirror Neuron System
§4.1 The Possible Role of the Mirror Neuron System in
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Action Understanding
§4.2 Criticism on the Role of the Mirror Neuron System in
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Action Understanding
§5 Empathy and the Mirror Neuron System
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§6 General Discussion
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Summary
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Literature
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§1 Introduction
Since the discovery of mirror neurons in Macaque monkeys there has been a lot of
speculation about the possibility of a similar mirror neuron system in humans and the
role of these neurons. One possible function of the mirror neurons could be the
understanding of actions made by others. The linkage of motor and sensor areas of the
brain could be the essential link in order to understand what somebody else is doing
and for what purpose he or she is doing it. Some researchers have also suggested that
empathy in humans is based on this mirror neuron system. For example, individuals
with Autism seem to have problems with social recognition and empathy. Deficits in
the mirror neuron system could be at the root of this problem. This thesis is aimed to
investigate mirror neurons and its possible role in action understanding and empathy.
In this paper it will be attempted to give an overview of the theories on this particular
subject and to give some insights on the mirror neuron system functioning. First of
all, the finding of mirror neurons in Macaque monkeys will be discussed together
with its possible function. Subsequently, the possibility of human mirror neurons will
be reviewed. Finally the role of the mirror neurons in action understanding and
empathy will be discussed.
§2 Mirror Neurons in Macaque Monkeys
The frontal cortex of monkeys consists of several areas, among which the F5 area is
especially of interest for its possible homology to Broca’s area in humans (Gallese,
Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti, Fadiga, Gallese & Fogassi, 1996). F5
is located in the ventro-rostral part of area 6. Stimulation and single cell recordings of
neurons within this area have been conducted and showed that it is associated with
hand and mouth movements (Hepp-Reymond, Hüsler, Maier & Qi, 1994; Rizzolatti,
Scandolara, Gentilucci & Camarda, 1981). In F5 hand movements are represented
more in the dorsal part and mouth movements are represented in the ventral part.
Rizzolatti et al. (1996) found in Macaque monkeys that some neurons in the
F5 area both fired during conduction of active movements and during observation of
the same movements made by the experimenter. A neuron with these particular
properties is called mirror neuron.
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§ 2.1 Properties of the Mirror Neurons
Gallese et al. (1996) conducted a single cell recording study in the F5 area, in which
they found that activation of mirror neurons was only caused by actions in which a
hand or mouth interacted with an object. Hand movements that included grasping,
manipulating and placing objects caused the strongest mirror neuron activation. The
showing of objects alone was not effective in activating the mirror neurons, even if
they were interesting stimuli like food items. Emotional gestures were also not
effective. These gestures involved threatening the monkey and the displaying of
unpleasant items. The use of tools, even if they were similar to the meaningful hand
movements, was not effective. If the monkey saw the experimenter use pliers to grasp
an object it did not activate the mirror neurons. Rizzolatti and Arbib (1998) showed
that the mirror neurons did fire after repetitive observation of a meaningful action
with a tool.
Gallese et al. (1996) also showed that it did not matter if the monkey executed
an action in a well-lit environment or in a dark environment. Therefore the mirror
neurons in the monkey did not merely fire while observing its own actions, because it
could not see the actions in the dark environment. This provided evidence that mirror
neurons did not exclusively respond to observed actions, but also to the execution of
actions.
Gallese et al. (1996) and Rizzolatti et al. (1996) showed that there is a
difference in the degree of congruence between mirror neurons. Strict congruent
mirror neurons have a very specific connection between the motor properties of the
neuron and the visual properties of the neuron. The relation in terms of general action
between the observed and executed movement, for example grasping with the hand, is
strict. Furthermore, they also have a strict relation in the manner in which the action
was executed. An example is a neuron that fires only when a precision grip movement
is performed with the hand. The other end of this spectrum consists of mirror neurons
that have no connection between their visual and motor properties. They are noncongruent. These mirror neurons respond for example both to the observation of
mouth and hand actions. The mirror neurons that are congruent, but not strict, are
considered as broadly congruent. An example of a broad congruent mirror neuron is a
neuron that fires both when a precision finger grasping movement is executed and
when it is observed, but also fires when a whole hand grasping movement is
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observed. Research has shown that 92% of mirror neurons are congruent,
approximately 30% are strict congruent, 60,9% is broadly congruent and 7,6% are
non-congruent.
The discharge of mirror neurons is not dependent of the distance of the
observed action. It has no effect on the discharge of mirror neurons if an observed
action is presented far away from or close by to the observer (Rizzolatti & Graighero,
2004).
§ 2.2 The Mirror Neuron System in Macaque Monkeys
Rizzolatti and Graighero (2004) state that other areas in the cortex of the Macaque
monkey besides F5 were found to have neurons that respond to observed actions
made by others. They suggest that there is a mirror neuron system (MNS) that has
different cortical areas that contain mirror neurons. First of all, the superior temporal
sulcus (STS) has neurons that respond to observed actions. This area sends output to
the ventral premotor cortex, including F5. In comparison with mirror neurons in F5
however, the STS neurons do not have motor properties.
Another cortical area where neurons were found that respond to actions made
by others is area 7b. It is located in the rostral part of the inferior parietal lobule. It
receives input from STS and sends output to the entire ventral premotor cortex. Some
neurons in the 7b area do have mirror neuron qualities. The MNS thus includes: The
rostral part of the inferior parietal lobule (7b) and the ventral premotor cortex
(including F5). STS, although related because of the input it sends to the MNS, is
strictly not a part of the MNS because it has no mirror neurons. Figure 1 shows the
monkey’s cortex and the areas of the MNS.
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Figure 1. The cortex of the Macaque monkey. Area F5 and 7b make up the core of the MNS. The STS is
linked with the MNS, but not a part of it. Adapted from Rizzolatti et al. (1996).
§2.3 The role of Mirror Neuron System in the Macaque Monkey
Looking at the possible functional role of the MNS, Gallese et al. (1996) and
Rizzolatti et al. (1996) proposed three possibilities. The first possibility is the
preparation of movement. The preparation of the execution of an action could benefit
from the fact that this action is observed before executing it. This makes it possible to
execute the action as fast as possible. However, if the mirror neurons were related
with the preparation of movement, they would continue firing between the
observation and movement. According to Gallese et al. (1996) the mirror neurons do
not continue firing in this period, thus it does not seem likely that the MNS is
involved in the preparation of movement. The second possibility is learning through
imitation. Human adults and children both learn trough imitation. Imitation could be
based on a mechanism that links the observation and execution of an action. Mirror
neurons could represent this link (Gallese et al., 1996). A study focused on imitation
of Macaque monkeys and found that newborn Macaque monkeys do imitate facial
gestures, but only for a short period of time. The MNS in macaque monkeys therefore
could be a system that provides a role in early imitation. However, it is not evident
that this role is still of importance in learning at a later age (Ferrari, Visalberghi,
Paukner, Fogassi, Ruggiero & Suomi, 2006). Finally, a possible function is the
understanding of observed action. If an observed action evokes a neural activity,
which is the same activity that would be produced when one executes a similar action,
the meaning of the observed action should be recognized. The similarity between the
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neural activities could be the mechanism behind this recognition.
A study provided evidence in favor of the action understanding theory. Even
while a meaningful object was hidden and the last part of a movement could not be
seen, some mirror neurons still fired. The monkeys saw beforehand if there was an
object present or not. Mirror neurons did not fire when the object was not present.
This shows that the motor representation of a meaningful action performed by another
can be generated internally in the premotor cortex of the observer (Umiltà, Kohler,
Gallese, Fogassi, Keysers & Rizzolati, 2001). In addition, researchers found that
mirror neuron activity was also present when a sound was played that previously was
paired with an action corresponding with the sound, e.g. ripping a piece of paper
(Kohler, Keysers, Umiltà, Fogassi, Gallese & Rizzolatti, 2002). Possibly, the motor
properties of that particular action were simulated in the monkey’s brain when only
the sound was presented. The visual stimuli were not needed. Kohler et al. (2002)
concluded that therefore the monkey ‘understood’ the action. However, it is difficult
to decide whether or not the monkey really understood the action, or that it had
associated the sound with the action through classical conditioning. The evidence is
indirect and it is difficult to say when a monkey really understands an action.
§3 Mirror Neurons in Humans
If indeed the mirror neurons in monkeys could be at the base of action understanding,
it could also be the case in humans. It could even be at the core of more complex
cognitive functions that makes humans understand each other and feel empathy. The
first thing to investigate is whether or not there are in fact mirror neurons in the
human cortex. The possibility of mirror neurons in humans was already proposed in
the first studies concerning mirror neurons of the Macaque monkey (Gallese et al.,
1996; Rizzolatti et al. 1996). So far, there are no single cell recordings of mirror
neurons in humans documented. Therefore there is no direct evidence of the existence
of mirror neurons in humans. There is, however, indirect evidence of the existence of
mirror neurons in humans (Rizzolatti & Graighero, 2004). Neurophysiological
experiments show that the motor cortex becomes active when observing others
performing an action, without the presence of overt motor activities (Rizzolatti &
Graighero, 2004).
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§3.1 Mirror Neurons in Humans
Fadiga, Fogassi, Pavesi and Rizzolatti (1995) found through Transcranial Magnetic
Stimulation (TMS) evidence in favor of the existence of mirror neurons in humans.
TMS is a non-invasive method of stimulating the nervous system. Through this
electric stimulation of the motor cortex they found enhanced motor evoked potentials
(MEPs) distinct from spontaneous potentials in hand and arm muscles of normal
human subjects while observing movement. The enhanced MEPs were only found
during conditions in which movement was shown. An interesting fact was that it did
not matter if the movements were transitive (movements with objects) or intransitive
(meaningless movements without objects). The increased potentials were only found
in the muscles that are active if a subject would execute the observed action. When
subjects merely observed the objects used in the transitive movement condition or a
dimming spotlight no MEPs were found. The dimming spotlight condition was added
to show non-human movement.
Maeda, Kleiner-Fishman and Pascual-Leone (2002) confirmed these findings
in a TMS study that focused on simple non-goal directed movements. They found that
there was enhancement of MEPs during observation of the action that was to be
executed. Seeing the movement of the index finger produced a larger MEP in the
muscles that would facilitate this movement. This provided evidence that the
observation of movements activates the motor cortex.
In an EEG study, Cochin, Barthelemy, Lejeune, Roux and Martineau (1998)
found that while observing human motion there was a desynchronization of the socalled Mu-rhythm of the spectrum of brain waves in the human cortex. This
desynchronization was not observed while observing a still scene (lake) or non-human
movement (waterfall). The desynchronization of the Mu-rythm is associated with
motor activity (Cochin et al., 1998). This study indicated that the motor cortex is
activated while observing human movement, but not while observing non-human
movement.
To investigate why there is no overt muscle activity mimicking the observed
action, Baldissera, Cavallari, Craighero and Fadiga (2001) focused on spinal cord
excitability. During the activation through TMS of a stretching reflex in a finger
muscle of the subject, the same or opposite action as the reflex was observed by the
subject. The same action was opening of the hand and the opposite action was closing
of the hand. The observation of the same action as the reflex caused the reflex to
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decrease in size. The cortical excitability increased when the same action was
observed, the spinal chord decreased. The spinal chord excitability therefore
contradicted the cortical excitability. This suggests that there is a spinal mechanism
that prevents the automatic overt mimicking of an observed action. Thus, the MNS
can be active without interfering with the normal muscular activity. Jeannerod (2001)
states that an inhibitory system could be present at the spinal chord level that coexists
with the cortical MNS to suppress overt movements.
The previous mentioned studies suggest that there is a MNS in humans. The
evidence is indirect, but Rizzolatti and Graighero (2004) state that it is likely that
there is an MNS in humans such as in Macaque monkeys. They proposed that the core
of the MNS in humans consists of two main regions. The first one is the rostral part of
the inferior parietal lobule (IPL) and the second region is located in the premotor
cortex, containing the lower part of the precentral gyrus and the posterior part of the
inferior frontal gyrus (IFG). The latter contains area 44, or Broca’s area. These areas
are predominantly motor areas, but are also active during observation of movement
(Rizzolatti & Graighero, 2004). Figure 2 shows the human MNS.
Figure 2. The human MNS, with the STS. Adapted from Iacoboni and Dapretto (2006).
The two main regions correspond with the regions of the MNS found in
monkeys. It is plausible that the IPL corresponds with the PF area in monkeys
(Rizzolatti & Craighero, 2004). F5 in monkeys is considered homologue to Broca’s
Area (Gallese et al., 1996). Therefore the areas of the MNS are consistent with the
areas of the Macaque monkey. The next step is to look at the properties of the human
MNS and the possible differences between the human and Macaque MNS.
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§3.2 Similarities and Differences between the Human and Macaque Monkey’s
Mirror Neuron System
Buccino et al. (2001) focused through fMRI on different parts of the premotor cortex
and the parietal lobule during the observation of a variety of movements. They found
that the MNS in humans is spatially organized, for a large range of movements. For
example, the same areas that were activated in the premotor cortex during an
execution of an arm movement are also activated during the observation of the same
arm movement. This is consistent with the amount of congruence in the monkey’s
mirror neurons (Gallese et al., 1996; Rizzolatti et al., 1996). It suggests that the MNS
is spatially organized and codes for specific actions made by specific effectors.
Buccino et al. (2001) also found that the IPL was only activated when a
transitive action was observed. An observation of a mimed or intransitive action did
not activate this area. The mimed action was the same action as the object-related
action, but without the object. This result supports the view that the parietal lobule has
a fundamental role in the description of objects for action (Jeannerod, 1994). It is also
consistent with the observation that the Macaque monkey’s MNS is only active
during the observation of transitive movements (Gallese et al., 1996; Rizzolatti et al.,
1996). However, Buccino et al. (2001) did find IFG activation during the observation
of mimed actions. Also, Maeda et al. (2002) found that the observation of intransitive
movements and transitive movements both showed enhanced MEPs. These results are
consistent with the earlier findings of Fadiga et al. (1995). This is a major difference
between the human and Macaque monkey’s MNS; the monkey’s MNS did not
respond to intransitive movements at all (Gallese et al., 1996; Rizzolatti et al., 1996).
The human brain area IFG, corresponding with F5, does respond to intransitive
actions.
This difference between the Macaque monkey’s MNS and the human MNS
could be based on the fact that Macaque monkeys do not use pantomime actions
(Iacoboni, 2009). Humans do use pantomime action in a lot of situations. For
example, a person mimes that he or she is going to sleep in some occasions by
pressing the hands together and placing the head against the hands. This could explain
the activation of mirror neurons during the observation of intransitive actions. The
MNS in humans exists of the areas that correspond with the monkey’s MNS
(Rizzolatti & Graighero, 2004). However, it could have evolved in humans in a
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different manner than in Macaque monkeys (Hickok, 2009).
§4 Action understanding and the Mirror Neuron System
Action understanding is defined as: “The capacity to achieve the internal description
of an action and to use it to organize appropriate future behavior” (Rizzolatti, Fogassi
& Gallese, 2001). The mirror neuron theory on action understanding is: When an
observed action evokes a neural activity which is normally evoked when the observed
action is executed, the meaning of the action is understood because of the similarity
between the two neural activities (Rizzolatti et al., 1996). Action understanding could
be mediated by the MNS.
§4.1 The Possible Role of the Mirror Neuron System in Action Understanding
To investigate the role of the MNS in action understanding, Buccino, Binkofski and
Riggio (2004) focused on the effect of the observation of different species that
performed similar actions. A subject observed humans, monkeys and dogs. The
observed action was either biting, or a specie-specific communicative action. Through
fMRI, they found that during the observation of biting the two main regions of the
human MNS were active, the IPL and the IFG. It did not matter what specie
performed the biting. It was different for the observation of communicative actions.
The frontal lobe was only activated during the observation of human (silent speech)
and monkey’s (silent lip smacking) communicative actions. The dog’s barking, also
silent, did not activate any frontal lobe activity. This indicates that different actions
can be processed differently. If an action is shown that is in the motor repertoire of the
person observing it, it is mapped on his or her motor system. The person recognizes
an action because he or she can perform the same action. It is therefore “personal
knowledge”. If an action is observed that is not in the motor repertoire, it is not
mapped in the motor system. The properties of this action are indentified on a visual
basis. Buccino et al. (2004) concluded that there seem to be two different means of
understanding action, one that involves some sort of ‘resonance’ in the motor areas of
the brain and one based more on visual information.
This study provides evidence for the role of the MNS in action understanding in
the sense that an internal description of the observed action is made, namely in the
areas of the MNS. If an action is observed that lies in the motor repertoire of the
observer the MNS is active and provides ‘motor resonance’. According to the mirror
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neuron theory of action understanding, this resonance should induce the
understanding of the action because of its neural similarity. The enhanced MEPs in
the muscles that would have been active during the execution of the observed action,
found through TMS studies, provide evidence for this statement (Baldissera et al.,
2001; Fadiga et al., 1995; Maedea et al., 2002). A spinal chord inhibition of the
muscles prevents overt mimicking of the action, allowing a functional motor
resonance in the cortex, provided through the MNS (Baldissera et al., 2001). The
question is: Is this internal description of the observed action necessary to understand
the action?
§4.2 Criticism on the role of the Mirror Neuron System in action understanding
Hickok (2009) interestingly pointed out, as a criticism of the study of Buccino et al.
(2004), that the lip smacking condition of the monkey holds less semantic information
than the silent speech condition and the barking dog condition. These last two
conditions are generally more present in everyday observations. The subjects
understood that the person they observed was speaking, they also understood that the
dog was barking. Lip smacking is in a lesser manner recognizable according to
Hickok (2009), yet it produced more MNS activity than the barking dog. Actions can
be understood without the MNS, the dog’s barking may be better understood than the
monkey’s lip smacking.
Catmur, Walsh and Heyes (2007) showed that the enhanced MEPs in the
activated muscles could be changed through exercise. Subjects were taught to perform
a movement of the little finger, while they observed the same movement of the index
finger on the screen. The MEPs recorded of the little finger muscles were enhanced
when an observation was made of the moving index finger and were not enhanced
while observing little finger movements. This contrasts the findings of Fadiga et al.
(1995). If the MNS was necessary in order to understand actions, the MEPs should
not change because it represents mirror neuron activity. This activity should cause the
person to understand the action before it produces his own action. The subjects
understood that the index finger was moving, but there was no mirror neuron activity
causing this understanding.
If the MNS is a necessary system to understand actions, deficits in the
production of actions should be correlated with deficits in action understanding.
Researchers focused on 37 patients with unilateral brain lesions causing apraxic
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impairments (Negri, Rumiati, Zadini, Ukmar, Mahon & Caramazza, 2007). The
patients were tested on several tasks concerning action understanding. Correlations
were found between, for example, pantomime imitation and pantomime recognition.
This suggests the relationship between the MNS and action recognition, because the
MNS was active during pantomime action (Buccino et al., 2001). However, there
were individual patients that did not support these correlations. Dissociation between
the individual patients caused Negri et al. (2007) to conclude that the ability to imitate
mimed actions is not necessary in able to recognize mimed actions. The absence of
working imitation skills did not disturb the action understanding. These findings
suggest that the MNS is not necessary in understanding actions. A point of criticism
on this study is that the patients had unilateral deficits. It cannot be excluded that the
partial damage could have influenced the results.
Lingnau, Gesierich and Caramazza (2009) concentrated, through fMRI, on
blood-oxygen level dependent (BOLD) response adaptation in the areas of the MNS
while first executing an action and then observing the same action. The adaptation
occurs when the same neurons are repeatedly used (Ogawa, Lee, Nayak & Glynn,
1990). So, if the MNS hypothesis of action understanding is true, this adaptation
should occur in the MNS whenever an action is first observed and then executed. It
should also occur when the action is first executed and then observed. Adaptation did
occur when the action was first observed and then executed or when two observations
were made after each other and also when two actions were executed after each other.
However, it did not occur when the action was first executed and then observed. This
lack of adaptation challenges the theory that action understanding is facilitated
through direct matching using the MNS.
A critical note on this research is that there is adaptation when the action is first
observed and then executed. Lignau et al. (2009) state that this could be helpful with
the preparation of the execution of a movement. Remember that Gallese et al. (1996)
excluded this possibility of the mirror neurons in Macaque monkeys, because there
was no mirror neuron activity in the time between the observation and execution of
movement. This raises questions on the interpretation of this adaptation.
Also, note that Lingnau et al. (2009) used intransitive movement in their study,
however as suggested earlier, to activate the entire MNS, transitive movements must
be used (Buccino et al., 2001). The authors however noticed that some mirror neurons
are active during intransitive actions. Earlier studies showed that there were enhanced
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MEPs during intransitive movements (Fadiga et al., 1995). Lignau et al. (2009)
further suggest that if the MNS is the key to understand actions, intransitive actions
should also produce MNS activity.
The mirror neurons are very interesting neurons in the sense of their double
role. They play a role in the observation of action and the execution of the same
action. Rizzolati et al. (1996) proposed that because of the neural similarities between
the observation and execution of an action, the action is understood. In the study of
Catmur et al. (2007) MEPs contradicted the expectations based on the mirror neuron
theory on action understanding. The neural activity between the observation and the
execution was not similar, but the subjects did understand the observed action. Negri
et al. (2007) showed that patients with deficits in the production of movement did not
necessarily have problems with the understanding of these movements. Thus the
neural similarity between the observation and execution of an action, as stated in the
theory of Rizzolatti et al. (1996), cannot be the only way to understand actions.
Does this mean that the MNS does not contribute to action understanding?
Haslinger et al. (2005) showed that there was more MNS activity in professional
pianists in contrast with naive controls while observing finger movements of a pianist.
It is conceivable that the expert pianist understands the observed action in a different
manner than the control. Perhaps the motor resonance enriches the experience of an
observation of an action, but the actual understanding does not depend on this motor
resonance.
Rizzolatti and Arbib (1998) showed that the MNS in Macaque monkeys could
adapt. It can be activated when observing an action with a tool, whereas it first was
not activated. Catmur et al. (2007) showed that the human MNS also could adapt.
Heyes (2010) suggests that the MNS could be formed through experience. It could be
a byproduct of associative learning, rather than a system designed for action
understanding. This theory is consistent with the evidence that the MNS can adapt to
new experiences. It is also consistent with the idea that we can understand actions
even if they are not in our motor repertoire. Seeing a dog barking does not activate the
MNS. We do however understand what the dog is doing. Also, if the dog is barking at
a certain time of the day, we have learned through experience that the dog wants to be
taken for a walk. Therefore we understand for what purpose the dog is barking.
Lignau et al. (2009) also suggested that the mirror neuron activity could be a
consequence of action understanding instead of the other way around. This is
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consistent with the MNS as a byproduct of associative learning. It is also consistent
with the findings of Kohler et al. (2002) in Macaque monkeys. They found that a
sound could activate the mirror neurons that are normally activated when a particular
action is observed. This sound could be linked with the action through experience and
therefore produce mirror neuron activity.
§5 Empathy and the Mirror Neuron System
Not only is action understanding regarded as a possible function of the MNS, another
function of the MNS in humans is proposed by Gallese (2003). He states that in a
similar manner as the theory on action understanding proposed by Rizzolatti et al.
(1996), the mirror neurons could be at the base of empathy. This theory was defined
earlier: When an observed action evokes a neural activity which is normally evoked
when the observed action is executed, the meaning of the action is understood
because of the similarity between the two neural activities. Gallese (2003) proposes
that the shared experience causes humans to understand each other. He calls this
shared experience the shared manifold, the ability of different organisms to
experience the same thing. He proposes that the MNS is the mechanism to share this
experience and ultimately cause us to understand others. He states that the mirror
neurons are not only used in order to understand each other’s actions, but also to
understand each other’s emotions and to empathize with another human being.
The first thing to notice is, that the mirror neurons in F5 of the Macaque
monkey’s brain were not active if emotional gestures were used (Gallese et al., 1996;
Rizzolatti et al., 1996). This means that if in humans the MNS is the underlying
system in order to feel empathy, the human mirror neurons must be evolved in a
different manner than in Macaque monkeys. This means that one must accept two
major differences between the Macaque monkey’s MNS and the human MNS: The
activation of the human MNS during intransitive actions and during emotional
gestures.
Gazolla, Aziz-Zadeh and Keysers (2006) found through fMRI that during the
exposure to sounds of actions, the same brain areas were active that were active
during the execution of the same actions. This provided evidence for human auditory
mirror neurons, in correspondence with Macaque monkey’s MNs (Kohler et al.,
2002). Furthermore, Gazzola et al. (2006) also found that individuals who scored
higher on an empathy scale showed stronger MNS activity. This provided some
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evidence that the MNS is linked with empathy. A critical note is that the number of
participants of this study was rather low (n=14). Also, the reason that the higher
scorers had more MNS activity is not fully understood. It could be that selective
attention to the actions made by others plays a role. High scorers may be more aware
of the actions of others and therefore have more MN activity. Therefore, this study
does not provide compelling evidence in favor of the theory stated by Gallese (2003).
If the MNS is the system that is responsible for empathy, the motor resonance
that causes the shared experience should be responsible for the understanding of
emotions (Gallese, 2003). Tamietto et al. (2009) focused on emotional contagion,
which is the tendency to pair our facial expressions with those of other individuals.
They used patients with unilateral damage to the visual cortex, causing affective
blindsight, and found that observing bodily expressions triggered the automatic reflex
of the emotion congruent facial muscles. Buccino et al. (2001) showed that the human
MNS is organized is such a manner that it responds very specific to the effectors, for
example hands, used in actions. The same reactions to different effectors therefore
must be caused outside of the MNS. Tamietto et al. (2009) also found emotionspecific pupil reactions that coincided with the facial expressions. There was no
evidence of motor activity prior to these reactions that could reflect motor resonance.
The responses were evoked through the affective meaning of the bodily expressions
and not through the motor properties of these expressions. This means that motor
resonance is not at the base of emotional contagion.
Another important conclusion from Tamietto et al. (2009) was that patients with
affective blindsight could effectively recognize the emotions that were presented in
the unseen visual field. The patients had automatic emotion-specific physical
reactions to the presented stimuli in the unseen visual field, which indicated emotional
changes. The recognition of emotions is an important point of the theory of Gallese
(2003) and is therefore challenged by these results. Tamietto et al. (2009) do notice
that it is not clear how this process works and that it needs more investigation in the
future.
Gazolla et al. (2006) state that individuals with autism spectrum disorder (ASD)
show weak MNS activity while observing others. A key impairment in individuals
with ASD is the disability to relate with another individual (Oberman, Ramachandran
& Pineda, 2008). The shared manifest proposed by Gallese (2003) states that in order
to feel empathy it is necessary to experience the same thing as another individual, thus
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to relate with another individual. This shared experience, formed by the MNS, allows
us to understand another person and to feel the same thing as somebody else. As
individuals with ASD cannot relate to each other in a normal manner, the MNS must
be impaired if the theory by Gallese (2003) is true.
Oberman et al. (2008) investigated the MNS in individuals with ASD. They
used EEG scans to investigate Mu-rhythm suppression. As discussed earlier, the Murhythm suppression is used to study the MNS in other studies (Cochin et al., 1998).
Oberman et al. (2008) let individuals with ASD watch videos of grasping movements
made by strangers or familiar individuals. They found that Mu-suppression does
occur in individuals with ASD if the actors of the movements were familiar to them.
This shows that the MNS in individuals with ASD is not impaired. It shows that the
MNS in this group of people is only active if a socially important individual performs
the action. The MNS is working but the activation of the MNS is impaired. The
question that is raised through this study is whether or not the decreased MNS activity
is the reason individuals suffer from ASD, or whether this decreased activity is caused
by an underlying deficit in relating to unfamiliar people.
§6 General discussion
Since the discovery of mirror neurons there has been a lot of discussion on the role of
these neurons. Gallese et al. (1996) focused on the role of the mirror neurons in action
understanding in Macaque monkeys and also in humans. The statement that the MNS
is the system underlying action understanding was quickly adopted in other studies.
Moreover, the role of the MNS was not restricted to action understanding, Gallese
(2003) states that the MNS is also the system that makes it possible to feel empathy
for another human being. This theory is built upon the basic idea that the mirror
neurons are necessary to understand actions. This thesis focused on the possible role
of the MNS in action understanding and also in empathy.
First off all, the MNS in humans must be different from the MNS in Macaque
monkeys. The human MNS is active during the observation of intransitive movements
(Buccino et al., 2001). It also must be active during emotional gestures to be the key
system in empathy (Gallese, 2003). Because of the fact there is no direct evidence that
a human MNS exists, the assumption must be made that if there is a MNS it is
evolved differently in humans than in Macaque monkeys.
Catmur et al. (2007) showed that the MNS activity could be changed through
15
exercise. Heyes (2010) pointed out that the MNS could be formed entirely through
associative learning. It means that the MNS exist because of action understanding and
not for action understanding. Evidence suggests that action understanding is possible
without the MNS. Therefore the MNS cannot be the necessary system contributing to
action understanding. It is however possible that the activation of the MNS enrich the
experience of the observation of an action (Hickok, 2009). Haslinger et al. (2005)
showed that expert pianists did have more MNS activity than novices, observing a
pianist playing. The expert pianists could have a different understanding of the
observation. Perhaps, the playing of the observed pianist is technically very good.
Only the expert pianist may recognize this fact.
If one does not accept the MNS as the necessary system responsible for action
understanding, than one must question the MNS as the necessary system for empathy.
This is because Gallese (2003) formed his hypothesis on the fact that the MNS is the
key in understanding actions. The low MNS activity in individuals with ASD has
been presented as evidence for the role of the MNS in empathy (Gazzola, 2006).
Oberman et al. (2008) showed that the MNS activity in individuals with ASD is
normal if someone familiar performs the action that is observed. Tamietto et al.
(2009) showed that emotional contagion is not achieved through the activity of the
MNS. They conclude that emotional contagion is achieved through the affective
meaning of the observed bodily or facial expressions, and that emotions are
recognized without the MNS. The MNS is therefore, in a similar manner as with
action understanding, not the necessary system that underlies empathy.
Heyes (2010) mentions that when a system is designed for a particular function,
such as the understanding of actions, the system tends to be specific in its function. A
byproduct tends have multiple uses and effects, but not necessary of sufficient to that
function. This is consistent with the idea of the MNS as a byproduct of associative
learning and not as a system designed for action understanding.
A lot of properties have been attributed to the MNS, including action
understanding and empathy. The basic idea of the MNS as a system responsible for
action understanding is not backed by strong evidence; therefore it might not be
justified. Building upon this statement, it can also not be justified to attribute the
ability to feel empathy through the MNS.
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Summary
This thesis focused on mirror neuron system in Macaque monkeys and in humans.
The focus is the function of this set of neurons. Firstly, the role of the mirror neuron
system on action understanding is discussed. The evidence suggests that the mirror
neuron system is not the necessary system for understanding actions. It might
contribute to action understanding, but this is not clear and needs further
investigation. The mirror neuron system is also linked to empathy in humans. The
evidence suggests that the mirror neuron system is not the necessary system for
feeling empathy. The mirror neuron system could be a byproduct of associative
learning.
17
Literature
Baldissera, F., Cavallari, P., Craighero, L., & Fadiga, L. (2001). Modulation of spinal
excitability during observation of hand actions in humans. European
Journal of Neuroscience, 13, 190-194.
Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., Seitz, R.
J., Zilles, K., Rizzolatti, G., & Freund, H.-J. (2001). Action observation
activates premotor and parietal areas in a somatotopic manner: An fMRI study.
European Journal of Neuroscience, 13, 400-404.
Buccino, G., Binkofski, F., & Riggio, L. (2004). The mirror neuron system and action
recognition. Brain and Language, 89, 370-376.
Catmur, C., Walsh, V., & Heyes, C. (2007). Sensimotor learning configures the
human mirror system. Current Biology, 17, 1527-1531.
Cochin, S., Barthelemy, C., Lejeune, B., Roux S., & Martineau, J. (1998). Perception
of motion and qEEG activity in human adults. Electroencephalography and
Clinical Neurophysiology, 107, 287-295.
Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during
action observation: A magnetic stimulation study. Journal of Neurophysiology,
73, 2608-2611.
Ferrari, P. F., Visalberghi, E., Paukner, A., Fogassi, L., Ruggiero, A., & Suomi, S. J.
(2006). Neonatal imitation in rhesus monkeys. PLoS Biology, 4, e302.
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G., (1996). Action recognition
in the premotor cortex. Brain, 119, 593-609.
Gallese, V., (2003). The roots of empathy: The shared manifold hypothesis and the
neural base of intersubjectivity. Psychopathology, 36, 171-180.
Gazolla, V., Aziz-Zadeh, L., & Keysers, C. (2006). Empathy and the somatotopic
auditory mirror system in humans. Current Biology, 16, 1824-1829.
Haslinger, B., Erhard, P., Altenmüller, E., Schroeder, U., Boecker, H., & CeballosBaumann, A. O. (2005). Transmodal sensimotor networks during action
observation in professional pianists. Journal of Cognitive Neuroscience, 17,
282-293.
Hepp-Reymond, M.-C., Hüsler, E. J., Maier, M.A., & Qi, H.-X. (1994). Force-related
activity in two regions of the primate ventral premotor cortex. Canadian
Journal of Physiology and Pharmacology, 72, 571-579.
18
Heyes, C. (2010). Where do mirror neurons come from? Neuroscience and
Biobehavioral Reviews, 34, 575-583.
Hickok, G. (2009). Eight problems for the mirror neuron theory of action
understanding in monkeys and humans. Journal of Cognitive Neuroscience, 21,
1229-1243.
Iacoboni, M., & Dapretto, M. (2006). The mirror neuron system and the consequences
of its dysfunction. Nature Reviews Neuroscience, 7, 942-951.
Iacoboni, M. (2009). Imitation, empathy and the mirror neurons. Annual Review of
Psychology, 60, 653-670.
Jeannerod, M., (1994). The representing brain: Neural correlates of motor intention
and imagery. Behavioral and Brain Sciences, 17, 187-202.
Jeannerod, M., (2001). Neural simulation of action: A unifying mechanism for motor
cognition. Neuroimage, 14, S103-S109.
Kohler, E., Keysers, C., Umiltà, M. A., Fogassi, L., Gallese, V., & Rizzolatti, G.,
(2002). Hearing sounds, understanding actions: Action representation in mirror
neurons. Science, 297, 846-848.
Lingnau, A., Gesierich, B., & Caramazza, A. (2009). Asymmetric fMRI adaption
reveals no evidence for mirror neurons in humans. Proceedings of the National
Academy of Sciences of the United States of America, 106, 9925-9930.
Maeda, F., Kleiner-Fishman, G., & Pascual-Leone, A. (2002). Motor facilitation
while observing hand actions: specificity of the effect and role of observer’s
orientation. Journal of Neurophysiology, 87, 1329-1335.
Negri, G. A., Rumiati, R. I., Zadini, A., Ukmar, M., Mahon, B. Z., & Caramazza, A.
(2007). What is the role of motor simulation in action and object recognition?
Evidence from apraxia. Cognitive Neuropsychology, 24, 795-816.
Oberman, L.M., Ramachandran, V.S., & Pineda, J. A. (2008). Modulation of mu
suppression in children with autism spectrum disorders in response to familiar
or unfamiliar stimuli: The mirror neuron hypothesis. Neuropsychologia, 46,
1558-1565.
Ogawa, S., Lee, T.-M., Nayak, A.S., & Glynn, P. (1990). Oxygenation-sensitive
contrast in magnetic resonance image of rodent brain at high magnetic fields.
Magnetic Resonance in Medicine, 14, 68-78.
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotors cortex and the
recognition of motor actions. Cognitive Brain Research, 3, 131-141.
19
Rizzolatti, G., & Arbib, M. A. (1998). Language within our grasp. Trends in
Neurosciences, 21, 188-194.
Rizzolatti, G., & Graighero, L. (2004). The mirror-neuron system. Annual Review of
Neuroscience, 27, 169-192.
Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms
underlying the understanding and imitation of action. Nature Reviews
Neuroscience, 2, 661-670.
Tamietto, M., Castelli, L., Vighetti, S., Perozzo, P., Geminiani, G., Weiskrantz L., &
de Gelder, B. (2009). Unseen facial and bodily expressions trigger fast
emotional reactions. Proceedings of the National Academy of Sciences of the
United States of America, 106, 17661-17666.
Umiltà, M., Kohler, E., Gallese, V., Fogassi, L., Keysers C., & Rizzolati, G. (2001).
I know what you are doing: A neurophysiological study. Neuron, 31, 155-165.
20