Iacoboni.

Existential Empathy:

The Intimacy of Self and Other

by Marco Iacoboni

Ahmanson-Lovelace Brain Mapping Center

Dept. of Psychiatry and Biobehavioral Sciences

Neuropsychiatric Institute

Brain Research Institute

David Geffen School of Medicine at UCLA

Address correspondence to:

Marco Iacoboni, MD PhD

Ahmanson Lovelace Brain Mapping Center
David Geffen School of Medicine at UCLA
660 Charles E. Young Drive South
Los Angeles, CA 90095, USA
iacoboni@loni.ucla.edu
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Recent studies in humans, inspired by single cell observations in macaques,

have described a neural architecture for imitation composed by three major

neural systems, the superior temporal cortex, the rostral part of the posterior

parietal cortex, and the inferior frontal cortex. This circuitry is connected to the

limbic system via the anterior sector of the insular lobe. This chapter reviews

empirical findings that suggest that imitation is a fundamental building block for

empathy and that in order to understand the emotional states of others we have

to activate the same neural systems activated by our own emotions. In principle,

these findings might be explained by a simulation theory of emotion, according to

which the subject witnessing emotions in others runs offline the same neural

routines used to express her/his emotions. However, an alternative account, that

I call the existential neuroscience account, is also plausible. Here, meaning of

any sort (thus, understanding emotions too) can emerge only through the

authentic commitment to other people's involvement in the world in which we are

thrown into. Thus, empathy via imitation is not a simulation made by an agent of

some mental states of other agents. Rather, it is the accomplishment of collective

agents.
 Iacoboni. 3

Empathy is the ability to imagine oneself in another's place, and understand the

other's feelings. The aspect of understanding the feelings of others defines

critically empathy, as opposed to sympathy, in which one has a feeling

corresponding to that which another feels. How does this understanding occur?

Understanding is the ability to make sense of things. As such, it is often assumed

that understanding is a mental ability. However, one of the background

assumptions of the research I am going to discuss here is that understanding is

not exclusively mental but is essentially corporeal as well. The other central

aspect of the definition of empathy is that it requires a sense of self and a sense

of the other. Without self awareness and awareness of the other, one cannot

'imagine oneself in another's place'. Thus, the foundational aspects of empathy

are a sense of self, a sense of the other, and an embodied relational process

between self and other. Such embodied relational process between self and

other can be easily identified in imitative behavior. Imitation is a central

component of non-verbal communication in pre-verbal toddlers. In fact, when

dyads and triads of children of different ages interact in settings with two or three

identical sets of attractive objects, imitation is the predominant form of interaction

between eighteen and thirty months of age (Nadel, 2002). The communicative

function of imitation is strongly suggested by a visible reduction of the effect of

setting – where identical objects are located such that imitation is favored – in

older children, for instance three-year-olds with verbal abilities (Nadel, 2002).

The role of imitation as a form of non-verbal communication actually continues in

adulthood, albeit in an automatic, largely non-conscious form. The phenomenon

 Iacoboni. 4

of the Chameleon effect has been described repeatedly and studied in several

labs (Barsalou, Niedenthal, Barbey, & Ruppert, 2003; Hatfield, Cacioppo, &

Rapson, 1994; Niedenthal, Barsalou, Winkielman, Krauth-Gruber, & Ric, in

press). It refers to non-conscious mimicry of the postures, mannerisms and facial

expressions of people while they interact in a social situation (Chartrand & Bargh,

1999; Hatfield et al., 1994). A series of experiments has shown not only that

people tend to imitate automatically and unintentionally the motor behavior of

strangers, but also that being imitated facilitates interactions and increases liking,

and that individual variability in the tendency to imitate others correlate with

scores on empathy (Chartrand & Bargh, 1999). What are the neural bases of

these phenomena?

In our lab, we have investigated in the last few years the neural

mechanisms of imitation and empathy. Our research has been inspired by

findings in single cell recording studies in macaques. These studies had revealed

functional properties in ventral premotor and inferior parietal neurons that

seemed quite relevant to imitation. In fact, these neurons, collectively called

mirror neurons, fire when the monkey performs object-oriented actions such as

grasping, holding, manipulating, tearing, and when the monkey sees somebody

else performing the same actions (diPellegrino, Fadiga, Fogassi, Gallese, &

Rizzolatti, 1992; Gallese, Fadiga, Fogassi, & Rizzolatti, 1996). Interestingly,

mirror neurons will not fire at the sight of a pantomimed action (Gallese et al.,

1996). However, mirror neurons fire even when the actual grasp of the object is

occluded from vision, as long as the animal has witnessed the initial reach of the
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hand going to grasp the object (Umilta et al., 2001). Moreover, mirror neurons

also fire, in complete darkness, at the sound associated with an action (Kohler et

al., 2002). The motor properties of these neurons are also interesting. In fact,

some of these neurons fire when the monkey grasps an object with the left hand,

or with the right hand, or with the mouth (Gallese et al., 1996). Taken together,

these data suggest that the firing of these neurons is associated with achieving

or witnessing the achievement of the goal of an action. Some mirror neurons in

the parietal lobe have complex properties that seem relevant to some higher

order aspects of motor behavior, for instance sequencing. It has been shown that

some parietal mirror neurons fire at the sight of a hand grasping an object and

fire also while the monkey bites the objects with the mouth (Gallese, Fogassi,

Fadiga, & Rizzolatti, 2002). This suggests a hand-to-mouth sequence. Mirror

neurons in the ventral premotor cortex are located in a cortical area called F5

(Matelli, Luppino, & Rizzolatti, 1985), whereas parietal mirror neurons are located

in a rostral inferior parietal area, area PF (Gallese et al., 2002). Area F5 and area

PF are reciprocally connected (Rizzolatti & Luppino, 2001). Area PF in the

inferior parietal lobule is in turn connected with the superior temporal cortex

(Seltzer & Pandya, 1994). In the superior temporal cortex, and precisely in the

superior temporal sulcus (STS), there are higher order visual neurons that fire at

the sight of object-oriented actions (Perrett et al., 1989). Similarly to the visual

properties of mirror neurons, these STS neurons do not fire at the sight of a hand

approaching a graspable object but not grasping it. The STS-PF-F5 circuit has

the anatomical connectivity pattern and the functional properties of a whole

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cortical circuit dedicated to the understanding of actions of self and other. Thus,

this circuit of the macaque brain seems a good candidate for being a precursor of

a similar system in the human brain relevant to imitation, a process that requires

the mapping of actions of others onto actions of self.

We tested this hypothesis in a series of brain imaging experiments largely

based on functional magnetic resonance imaging (fMRI). The rationale behind

the studies was the following: if one looks at the activity in mirror neurons during

execution and observation of action, the firing rate during observation is

approximately half the firing rate recorded during execution of action (Gallese et

al., 1996). Thus, we predicted that areas with mirror properties in the human

brain should have an increased signal during motor execution - compared to a

resting baseline - twice as large as the one obtained during observation of action.

Moreover, given that imitation yields both observation and execution of an action,

we posited that in mirror areas the increased signal during imitation should

amount to approximately the sum of the increased signal during execution only

and observation only. This profile of activity was observed in pars opercularis of

the inferior frontal gyrus and in the rostral part of the posterior parietal cortex

during imitation of finger movements (Iacoboni et al., 1999). These two regions

are anatomically compatible with the macaque regions containing mirror neurons,

area F5 in the inferior frontal cortex and area PF in the rostral part of the

posterior parietal cortex. With regard to the human homologue of macaque STS,

several labs have independently reported that posterior STS in the human brain

responds to biological motion (Allison, Puce, & McCarthy, 2000; Puce, Allison,
 Iacoboni. 7

Bentin, Gore, & McCarthy, 1998; Puce & Perrett, 2003). In our imitation studies

we also observed an area in posterior STS that responded more to biological

motion than to static pictures of hands. Importantly, this region seems

functionally connected to fronto-parietal mirror areas in that it seems the

recipients of efferent copies of motor commands originating from fronto-parietal

mirror areas (Iacoboni et al., 2001). Efferent copies of motor commands are

useful to predict the sensory consequences of planned actions. Given that STS

seems to provide a higher order description of the action to be imitated, we

proposed that when STS receives efferent copies of motor commands during

imitation, it performs a matching process between the visual description of the

action and the predicted sensory consequences of the planned imitative action

(Iacoboni et al., 2001).

We have also proposed that the activity in the inferior frontal region with

mirror properties, most likely Brodmann area 44, is associated with the goal of

the imitative action (Iacoboni et al., 1999). In fact, the activity in Brodmann area

44 is reliably higher during imitation of actions with visible goals compared to

actions with no visible goal, even though the motor aspect of the action is

identical in both cases (Koski et al., 2002). Interestingly, Brodmann area 44 also

shows higher activity during imitation of action as in a mirror – for instance, when

model and imitator are face to face, the model is using the left hand while the

imitator is imitating with the right hand - compared to imitation of the same action

with the anatomically corresponding hand - for instance, when model and imitator

are face to face, the model is using the right hand while the imitator is imitating
 Iacoboni. 8

with the right hand. Imitating as in a mirror is the predominant form of imitation

early in development (Wapner & Cirillo, 1968). In this form of imitation, the model

and the imitator share the same sector of space, they get physically closer.

Taken together, this evidence suggests that one of the goals of the imitative

process is to create some form of intimacy between the model and the imitator.

This concept of intimacy fits well with the links between imitation and empathy

and it has been largely neglected in the behavioral studies of imitation of the last

decades that were dominated by a cold, cognitive approach to the investigation

of imitative behavior. But so far we have described cortical areas that are

relevant to imitation and do not seem to belong to the classical neural systems

associated with emotions. So, the question we decided to address was the

following: how does the cortical architecture for imitation composed by STS,

rostral part of the posterior parietal cortex and inferior frontal cortex connect

anatomically and functionally with areas classically linked to emotional behavior?

To address this question we first looked at the available anatomical

evidence. In the primate brain there seems to be at least one area connecting the

limbic system with the three cortical systems – superior temporal cortex,

posterior parietal cortex and inferior frontal cortex - that are critical to imitation.

This area is the dysgranular sector of the insular lobe (Augustine, 1996). We

posited that the dysgranular sector of the insula might play a key role in a large-

scale neural network for empathy comprising areas relevant to emotion and to

imitation. This hypothesis fulfilled the original proposal of Lipps (as cited by

(Gallese, 2001), according to which a form of inner imitation of the action of

 Iacoboni. 9

others was critical to generate empathy. This hypothesis was also supported by

evidence suggesting that the insula receives slow-conducting unmyelinated

fibers that respond to caress-light touch and may be relevant to emotional and

affiliative behavior between individuals (Olausson et al., 2002). To test

empirically this model, we used fMRI while subjects were either observing or

imitating facial emotional expressions. We reasoned that if the way to empathy

goes through some forms of inner imitation of actions of others, then even the

simple observation of emotional facial expression should activated the same

brain regions used to perform and imitate those emotional facial expressions.

However, overt imitation of those emotional facial expressions should yield

greater activity in this large-scale network comprising the human homologues of

monkey STS, PF, and F5, the insula, and the limbic system due to the

simultaneous encoding of the sensory input and planning of the motor output

(Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003). We did observe such pattern

of activity in this neural circuit (Carr et al., 2003). Of particular interest is that the

limbic area that demonstrated the predicted pattern of activity was the right

amygdala. A study on conscious and unconscious processing of emotional facial

expression had suggested that the right amygdala is associated with

unconscious processing of emotional facial expressions (Morris, Ohman, &

Dolan, 1998). This is in line with the kind of unconscious imitation observed in

empathic individuals (Chartrand & Bargh, 1999) and suggests that the kind of

empathic mechanism we are tapping into here does not require an explicit

representational content of the emotional states of others.

 Iacoboni. 10

In this first study on imitating emotional facial expressions we treated

different emotions as a single entity, but different emotions are obviously not a

single entity and often are associated with different neural systems. In a large-

scale study on emotions in adolescence that we are currently performing we are

now comparing observation and imitation of different kinds of emotions. An

interesting preliminary finding of some interim analyses show that when subjects

- in this case 21 ten-year-old children with no neurological or psychiatric disorder

- imitate a happy face, there is increased activity in medial prefrontal cortex,

encompassing also the orbitofrontal sector, compared to imitating a face with a

neutral emotional expression (Figure 1). The medial part of the orbitofrontal

cortex has been associated with monitoring the reward value of different kinds of

reinforcers (Kringelbach & Rolls, 2004). Indeed, also the ventral striatum,

strongly associated with reward value, was activated by this contrast. Imitating a

happy face of others seems for the self a rewarding experience. The self enjoys

participating with a resonant bodily expression to the happiness of others. Again,

the intimacy of self and other seems transparent during empathic resonance.

Interestingly, several studies on the sense of self have used a technique

called the morphing technique, according to which the face of self and the face of

various kinds of others are morphed in a single face to varying degrees. This

technique has been prevalently used in tasks requiring self-recognition, rather

than any form of empathic resonance. Surprisingly, in a recent study on self-

recognition from our group using fMRI and the morphing technique we observed

a clear-cut involvement of the mirror system in recognizing morphs prevalently

 Iacoboni. 11

made of self. In this experiment, we used morphs composed only of self and

highly familiar others (people that spent several hours a day with the subjects or

were long-time close friends of the subjects). Previous studies of this kind had

mostly adopted the approach of using as others famous people. With this

approach, one controls nicely for familiarity of the stimulus, because presumably

a face of a famous person is a face that subjects had seen several times.

However, this approach does not control for the significance of the other to the

self. If there is no personal relationship with the other, the other is probably

perceived in a detached way. In contrast, when the other is a highly familiar

person, the perception of the other is presumably linked to a sense of

engagement, commitment, closeness, and intimacy. In our study, where the

other was always represented by a highly familiar personal friend, self-

recognition of morphs was associated with increased activity in frontal and

parietal mirror areas in the right hemisphere (Figure 2) for increasing percentage

of self in the morph (Uddin, Kaplan, Molnar-Szakacs, Zaidel, & Iacoboni,

submitted). That is, the greater the contribution of self in the morph, the greater

the increase of signal in fronto-parietal mirror areas. How do we explain this

signal increase in mirror areas during self-recognition of morphs of self and

highly personally familiar other? After all, mirror areas map actions of others onto

actions of self, and at prima facie they seem to support a mechanism for

assimilating self and other, rather than a mechanism for distinguishing them.

However, it has been shown that even passive viewing of a static face activates

premotor activity (Leslie, Johnson-Frey, & Grafton, 2004). Thus, watching a face
 Iacoboni. 12

seems to induce some form of motor imagery. Here, when subjects watch

morphs composed of self and highly familiar and personally close others, mirror

areas are activated due to the highly relevant social relation of self and other and

more so for morphs composed prevalently by self because of the ease with

which one can map oneself onto one's own motor system. What emerges from

this study is a sense that notions like self and other cannot be assimilated to

static representations, but are actually highly dynamic and interdependent. Mirror

areas seem to monitor this inter-dependence, this intimacy, this sense of

collective agency that comes out of social interactions and that is tightly linked to

the ability to form empathic resonance (Chartrand & Bargh, 1999). Rather than

the product of a Cartesian self that contemplates others and infer their emotional

states, or the other kind of Cartesian self that simulates the emotional states of

others by activating the same neural system that would be activated when

personally feeling those emotions, mirror activity linking self and other

emotionally and empathically seem to support the view of an existential self that

understands the emotional states of other people by committing authentically to

other people's involvement in the world in which the self is thrown into. Thus,

empathy, and especially empathy via imitation, as we have seen above, is not a

simulation made by an agent of some mental states of other agents. Rather, it is

the accomplishment of collective agents.

 Iacoboni. 13

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 Iacoboni. 17

Figure 1. In a study on 21 adolescents imitating facial emotional expressions, in

which gender and race were equally balanced across emotions, medial

orbitofrontal (MOFC) and ventral striatum were more active for imitating a happy

face compared to imitating a face with a neutral facial expression.

 Iacoboni. 18

Figure 2. Increased activity in right inferior frontal and rostral inferior parietal

areas during a self-recognition task while watching morphs of self and other

faces composed prevalently by self.