Fluent Essays

Assist with discussion Discussion 8 Part 1 Read “Mirror neurons and their function in cognitively understood Empathy” , and then discuss, in general terms, what the mirror neurons system is (using the article as a primary source). Are there certain parts of the brain that have a higher number of these cells? Also consider how plasticity relates to this. In other words, is it possible that mirror neurons are the product of the environment to a certain extent? Support your responses. Discussion 8 Part 2 Read “THE MIRROR-NEURON SYSTEM”, and then discuss the purpose, general methods, main results, and significance of the studies. Considering the function of empathy from the perspective of a cognitive neuroscientist, what adaptive functions could empathy serve? Also, consider the implications of lacking empathy. 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 10.1146/annurev.neuro.27.070203.144230 Annu. Rev. Neurosci. 2004. 27:169–92 doi: 10.1146/annurev.neuro.27.070203.144230 Copyright c© 2004 by Annual Reviews. All rights reserved First published online as a Review in Advance on March 5, 2004 THE MIRROR-NEURON SYSTEM Giacomo Rizzolatti1 and Laila Craighero2 1Dipartimento di Neuroscienze, Sezione di Fisiologia, via Volturno, 3, Università di Parma, 43100, Parma, Italy; email: [email protected]; 2Dipartimento SBTA, Sezione di Fisiologia Umana, via Fossato di Mortara, 17/19, Università di Ferrara, 44100 Ferrara, Italy; email: [email protected] Key Words mirror neurons, action understanding, imitation, language, motor cognition � Abstract A category of stimuli of great importance for primates, humans in particular, is that formed by actions done by other individuals. If we want to survive, we must understand the actions of others. Furthermore, without action understanding, social organization is impossible. In the case of humans, there is another faculty that depends on the observation of others’ actions: imitation learning. Unlike most species, we are able to learn by imitation, and this faculty is at the basis of human culture. In this review we present data on a neurophysiological mechanism—the mirror-neuron mechanism—that appears to play a fundamental role in both action understanding and imitation. We describe first the functional properties of mirror neurons in monkeys. We review next the characteristics of the mirror-neuron system in humans. We stress, in particular, those properties specific to the human mirror-neuron system that might explain the human capacity to learn by imitation. We conclude by discussing the relationship between the mirror-neuron system and language. INTRODUCTION Mirror neurons are a particular class of visuomotor neurons, originally discovered in area F5 of the monkey premotor cortex, that discharge both when the monkey does a particular action and when it observes another individual (monkey or human) doing a similar action (Di Pellegrino et al. 1992, Gallese et al. 1996, Rizzolatti et al. 1996a). A lateral view of the monkey brain showing the location of area F5 is presented in Figure 1. The aim of this review is to provide an updated account of the functional properties of the system formed by mirror neurons. The review is divided into four sections. In the first section we present the basic functional properties of mirror neurons in the monkey, and we discuss their functional roles in action understanding. In the second section, we present evidence that a mirror-neuron system similar to that of the monkey exists in humans. The third section shows that in humans, in addition to action understanding, the mirror-neuron system plays a fundamental role in action imitation. The last section is more speculative. 0147-006X/04/0721-0169$14.00 169 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 170 RIZZOLATTI � CRAIGHERO We present there a theory of language evolution, and we discuss a series of data supporting the notion of a strict link between language and the mirror-neuron system (Rizzolatti & Arbib 1998). THE MIRROR-NEURON SYSTEM IN MONKEYS F5 Mirror Neurons: Basic Properties There are two classes of visuomotor neurons in monkey area F5: canonical neurons, which respond to the presentation of an object, and mirror neurons, which respond when the monkey sees object-directed action (Rizzolatti & Luppino 2001). In order to be triggered by visual stimuli, mirror neurons require an interaction between a biological effector (hand or mouth) and an object. The sight of an object alone, of an agent mimicking an action, or of an individual making intransitive (nonobject- directed) gestures are all ineffective. The object significance for the monkey has no obvious influence on the mirror-neuron response. Grasping a piece of food or a geometric solid produces responses of the same intensity. Mirror neurons show a large degree of generalization. Presenting widely differ- ent visual stimuli, but which all represent the same action, is equally effective. For example, the same grasping mirror neuron that responds to a human hand grasping an object responds also when the grasping hand is that of a monkey. Similarly, the response is typically not affected if the action is done near or far from the monkey, in spite of the fact that the size of the observed hand is obviously different in the two conditions. It is also of little importance for neuron activation if the observed action is even- tually rewarded. The discharge is of the same intensity if the experimenter grasps the food and gives it to the recorded monkey or to another monkey introduced in the experimental room. An important functional aspect of mirror neurons is the relation between their visual and motor properties. Virtually all mirror neurons show congruence between the visual actions they respond to and the motor responses they code. According to the type of congruence they exhibit, mirror neurons have been subdivided into “strictly congruent” and “broadly congruent” neurons (Gallese et al. 1996). Mirror neurons in which the effective observed and effective executed actions correspond in terms of goal (e.g., grasping) and means for reaching the goal (e.g., precision grip) have been classed as “strictly congruent.” They represent about one third of F5 mirror neurons. Mirror neurons that, in order to be triggered, do not require the observation of exactly the same action that they code motorically have been classed as “broadly congruent.” They represent about two thirds of F5 mirror neurons. F5 Mouth Mirror Neurons The early studies of mirror neurons concerned essentially the upper sector of F5 where hand actions are mostly represented. Recently, a study was carried out on 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH MIRROR NEURONS 171 the properties of neurons located in the lateral part of F5 (Ferrari et al. 2003), where, in contrast, most neurons are related to mouth actions. The results showed that about 25\% of studied neurons have mirror properties. According to the visual stimuli effective in triggering the neurons, two classes of mouth mirror neurons were distinguished: ingestive and communicative mirror neurons. Ingestive mirror neurons respond to the observation of actions related to in- gestive functions, such as grasping food with the mouth, breaking it, or sucking. Neurons of this class form about 80\% of the total amount of the recorded mouth mirror neurons. Virtually all ingestive mirror neurons show a good correspondence between the effective observed and the effective executed action. In about one third of them, the effective observed and executed actions are virtually identical (strictly congruent neurons); in the remaining, the effective observed and executed actions are similar or functionally related (broadly congruent neurons). More intriguing are the properties of the communicative mirror neurons. The most effective observed action for them is a communicative gesture such as lip smacking, for example. However, from a motor point of view they behave as the ingestive mirror neurons, strongly discharging when the monkey actively performs an ingestive action. This discrepancy between the effective visual input (communicative) and the effective active action (ingestive) is rather puzzling. Yet, there is evidence suggest- ing that communicative gestures, or at least some of them, derived from ingestive actions in evolution (MacNeilage 1998, Van Hoof 1967). From this perspective one may argue that the communicative mouth mirror neurons found in F5 reflect a process of corticalization of communicative functions not yet freed from their original ingestive basis. The Mirror-Neuron Circuit Neurons responding to the observation of actions done by others are present not only in area F5. A region in which neurons with these properties have been de- scribed is the cortex of the superior temporal sulcus (STS; Figure 1) (Perrett et al. 1989, 1990; Jellema et al. 2000; see Jellema et al. 2002). Movements effective in eliciting neuron responses in this region are walking, turning the head, bending the torso, and moving the arms. A small set of STS neurons discharge also during the observation of goal-directed hand movements (Perrett et al. 1990). If one compares the functional properties of STS and F5 neurons, two points emerge. First, STS appears to code a much larger number of movements than F5. This may be ascribed, however, to the fact that STS output reaches, albeit indirectly (see below), the whole ventral premotor region and not only F5. Second, STS neurons do not appear to be endowed with motor properties. Another cortical area where there are neurons that respond to the observation of actions done by other individuals is area 7b or PF of Von Economo (1929) (Fogassi et al. 1998, Gallese et al. 2002). This area (see Figure 1) forms the rostral part of the 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 172 RIZZOLATTI � CRAIGHERO inferior parietal lobule. It receives input from STS and sends an important output to the ventral premotor cortex including area F5. PF neurons are functionally heterogeneous. Most of them (about 90\%) respond to sensory stimuli, but about 50\% of them also have motor properties discharging when the monkey performs specific movements or actions (Fogassi et al. 1998, Gallese et al. 2002, Hyvarinen 1982). PF neurons responding to sensory stimuli have been subdivided into “so- matosensory neurons” (33\%), “visual neurons” (11\%), and “bimodal (somatosen- sory and visual) neurons” (56\%). About 40\% of the visually responsive neurons respond specifically to action observation and of them about two thirds have mirror properties (Gallese et al. 2002). In conclusion, the cortical mirror neuron circuit is formed by two main regions: the rostral part of the inferior parietal lobule and the ventral premotor cortex. STS is strictly related to it but, lacking motor properties, cannot be considered part of it. Function of the Mirror Neuron in the Monkey: Action Understanding Two main hypotheses have been advanced on what might be the functional role of mirror neurons. The first is that mirror-neuron activity mediates imitation (see Jeannerod 1994); the second is that mirror neurons are at the basis of action understanding (see Rizzolatti et al. 2001). Both these hypotheses are most likely correct. However, two points should be specified. First, although we are fully convinced (for evidence see next section) that the mirror neuron mechanism is a mechanism of great evolutionary importance through which primates understand actions done by their conspecifics, we cannot claim that this is the only mechanism through which actions done by others may be understood (see Rizzolatti et al. 2001). Second, as is shown below, the mirror- neuron system is the system at the basis of imitation in humans. Although laymen are often convinced that imitation is a very primitive cognitive function, they are wrong. There is vast agreement among ethologists that imitation, the capacity to learn to do an action from seeing it done (Thorndyke 1898), is present among primates, only in humans, and (probably) in apes (see Byrne 1995, Galef 1988, Tomasello & Call 1997, Visalberghi & Fragaszy 2001, Whiten & Ham 1992). Therefore, the primary function of mirror neurons cannot be action imitation. How do mirror neurons mediate understanding of actions done by others? The proposed mechanism is rather simple. Each time an individual sees an action done by another individual, neurons that represent that action are activated in the observer’s premotor cortex. This automatically induced, motor representation of the observed action corresponds to that which is spontaneously generated during active action and whose outcome is known to the acting individual. Thus, the mirror system transforms visual information into knowledge (see Rizzolatti et al. 2001). 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH MIRROR NEURONS 173 Evidence in Favor of the Mirror Mechanism in Action Understanding At first glance, the simplest, and most direct, way to prove that the mirror-neuron system underlies action understanding is to destroy it and examine the lesion effect on the monkey’s capacity to recognize actions made by other monkeys. In practice, this is not so. First, the mirror-neuron system is bilateral and includes, as shown above, large portions of the parietal and premotor cortex. Second, there are other mechanisms that may mediate action recognition (see Rizzolatti et al. 2001). Third, vast lesions as those required to destroy the mirror neuron system may produce more general cognitive deficits that would render difficult the interpretation of the results. An alternative way to test the hypothesis that mirror neurons play a role in action understanding is to assess the activity of mirror neurons in conditions in which the monkey understands the meaning of the occurring action but has no access to the visual features that activate mirror neurons. If mirror neurons mediate action understanding, their activity should reflect the meaning of the observed action, not its visual features. Prompted by these considerations, two series of experiments were carried out. The first tested whether F5 mirror neurons are able to recognize actions from their sound (Kohler et al. 2002), the second whether the mental representation of an action triggers their activity (Umiltà et al. 2001). Kohler et al. (2002) recorded F5 mirror neuron activity while the monkey was observing a noisy action (e.g., ripping a piece of paper) or was presented with the same noise without seeing it. The results showed that about 15\% of mirror neurons responsive to presentation of actions accompanied by sounds also responded to the presentation of the sound alone. The response to action sounds did not depend on unspecific factors such as arousal or emotional content of the stimuli. Neurons re- sponding specifically to action sounds were dubbed “audio-visual” mirror neurons. Neurons were also tested in an experimental design in which two noisy actions were randomly presented in vision-and-sound, sound-only, vision-only, and motor conditions. In the motor condition, the monkeys performed the object-directed action that they observed or heard in the sensory conditions. Out of 33 studied neurons, 29 showed auditory selectivity for one of the two hand actions. The selectivity in visual and auditory modality was the same and matched the preferred motor action. The rationale of the experiment by Umiltà et al. (2001) was the following. If mirror neurons are involved in action understanding, they should discharge also in conditions in which monkey does not see the occurring action but has sufficient clues to create a mental representation of what the experimenter does. The neurons were tested in two basic conditions. In one, the monkey was shown a fully visible action directed toward an object (“full vision” condition). In the other, the monkey saw the same action but with its final, critical part hidden (“hidden” condition). Before each trial, the experimenter placed a piece of food behind the screen so 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 174 RIZZOLATTI � CRAIGHERO that the monkey knew there was an object there. Only those mirror neurons were studied that discharged to the observation of the final part of a grasping movement and/or to holding. Figure 2 shows the main result of the experiment. The neuron illustrated in the figure responded to the observation of grasping and holding (A, full vision). The neuron discharged also when the stimulus-triggering features (a hand approaching the stimulus and subsequently holding it) were hidden from monkey’s vision (B, hidden condition). As is the case for most mirror neurons, the observation of a mimed action did not activate the neuron (C, full vision, and D, hidden condition). Note that from a physical point of view B and D are identical. It was therefore the understanding of the meaning of the observed actions that determined the discharge in the hidden condition. More than half of the tested neurons discharged in the hidden condition. Out of them, about half did not show any difference in the response strength between the hidden- and full-vision conditions. The other half responded more strongly in the full-vision condition. One neuron showed a more pronounced response in the hidden condition than in full vision. In conclusion, both the experiments showed that the activity of mirror neurons correlates with action understanding. The visual features of the observed actions are fundamental to trigger mirror neurons only insomuch as they allow the under- standing of the observed actions. If action comprehension is possible on another basis (e.g., action sound), mirror neurons signal the action, even in the absence of visual stimuli. THE MIRROR-NEURON SYSTEM IN HUMANS There are no studies in which single neurons were recorded from the putative mirror-neuron areas in humans. Thus, direct evidence for the existence of mirror neurons in humans is lacking. There is, however, a rich amount of data proving, indirectly, that a mirror-neuron system does exist in humans. Evidence of this comes from neurophysiological and brain-imaging experiments. Neurophysiological Evidence Neurophysiological experiments demonstrate that when individuals observe an action done by another individual their motor cortex becomes active, in the absence of any overt motor activity. A first evidence in this sense was already provided in the 1950s by Gastaut and his coworkers (Cohen-Seat et al. 1954, Gastaut & Bert 1954). They observed that the desynchronization of an EEG rhythm recorded from central derivations (the so-called mu rhythm) occurs not only during active movements of studied subjects, but also when the subjects observed actions done by others. This observation was confirmed by Cochin et al. (1998, 1999) and by Altschuler et al. (1997, 2000) using EEG recordings, and by Hari et al. (1998) using 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH MIRROR NEURONS 175 magnetoencephalographic (MEG) technique. This last study showed that the desyn- chronization during action observation includes rhythms originating from the cor- tex inside the central sulcus (Hari & Salmelin 1997, Salmelin & Hari 1994). More direct evidence that the motor system in humans has mirror properties was provided by transcranial magnetic stimulation (TMS) studies. TMS is a non- invasive technique for electrical stimulation of the nervous system. When TMS is applied to the motor cortex, at appropriate stimulation intensity, motor-evoked potentials (MEPs) can be recorded from contralateral extremity muscles. The am- plitude of these potentials is modulated by the behavioral context. The modu- lation of MEPs’ amplitude can be used to assess the central effects of various experimental conditions. This approach has been used to study the mirror neuron system. Fadiga et al. (1995) recorded MEPs, elicited by stimulation of the left motor cortex, from the right hand and arm muscles in volunteers required to observe an experimenter grasping objects (transitive hand actions) or performing meaningless arm gestures (intransitive arm movements). Detection of the dimming of a small spot of light and presentation of 3-D objects were used as control conditions. The results showed that the observation of both transitive and intransitive actions determined an increase of the recorded MEPs with respect to the control conditions. The increase concerned selectively those muscles that the participants use for producing the observed movements. Facilitation of the MEPs during movement observation may result from a fa- cilitation of the primary motor cortex owing to mirror activity of the premotor areas, to a direct facilitatory input to the spinal cord originating from the same areas, or from both. Support for the cortical hypothesis (see also below, Brain Imaging Experiments) came from a study by Strafella & Paus (2000). By using a double-pulse TMS technique, they demonstrated that the duration of intracortical recurrent inhibition, occurring during action observation, closely corresponds to that occurring during action execution. Does the observation of actions done by others influence the spinal cord ex- citability? Baldissera et al. (2001) investigated this issue by measuring the size of the H-reflex evoked in the flexor and extensor muscles of normal volunteers during the observation of hand opening and closure done by another individual. The results showed that the size of H-reflex recorded from the flexors increased during the observation of hand opening, while it was depressed during the ob- servation of hand closing. The converse was found in the extensors. Thus, while the cortical excitability varies in accordance with the seen movements, the spinal cord excitability changes in the opposite direction. These findings indicate that, in the spinal cord, there is an inhibitory mechanism that prevents the execution of an observed action, thus leaving the cortical motor system free to “react” to that action without the risk of overt movement generation. In a study of the effect of hand orientation on cortical excitability, Maeda et al. (2002) confirmed (see Fadiga et al. 1995) the important finding that, in humans, intransitive movements, and not only goal-directed actions, determine 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 176 RIZZOLATTI � CRAIGHERO motor resonance. Another important property of the human mirror-neuron system, demonstrated with TMS technique, is that the time course of cortical facilitation during action observation follows that of movement execution. Gangitano et al. (2001) recorded MEPs from the hand muscles of normal volunteers while they were observing grasping movements made by another individual. The MEPs were recorded at different intervals following the movement onset. The results showed that the motor cortical excitability faithfully followed the grasping movement phases of the observed action. In conclusion, TMS studies indicate that a mirror-neuron system (a motor res- onance system) exists in humans and that it possesses important properties not observed in monkeys. First, intransitive meaningless movements produce mirror- neuron system activation in humans (Fadiga et al. 1995, Maeda et al. 2002, Patuzzo et al. 2003), whereas they do not activate mirror neurons in monkeys. Second, the temporal characteristics of cortical excitability, during action observation, suggest that human mirror-neuron systems code also for the movements forming an action and not only for action as monkey mirror-neuron systems do. These properties of the human mirror-neuron system should play an important role in determining the humans’ capacity to imitate others’ action. Brain Imaging Studies: The Anatomy of the Mirror System A large number of studies showed that the observation of actions done by others activates in humans a complex network formed by occipital, temporal, and parietal visual areas, and two cortical regions whose function is fundamentally or predom- inantly motor (e.g., Buccino et al. 2001; Decety et al. 2002; Grafton et al. 1996; Grèzes et al. 1998; Grèzes et al. 2001; Grèzes et al. 2003; Iacoboni et al. 1999, 2001; Koski et al. 2002, 2003; Manthey et al. 2003; Nishitani & Hari 2000, 2002; Perani et al. 2001; Rizzolatti et al. 1996b). These two last regions are the rostral part of the inferior parietal lobule and the lower part of the precentral gyrus plus the posterior part of the inferior frontal gyrus (IFG). These regions form the core of the human mirror-neuron system. Which are the cytoarchitectonic areas that form these regions? Interpretation of the brain-imaging activations in cytoarchitectonic terms is always risky. Yet, in the case of the inferior parietal region, it is very plausible that the mirror activation corresponds to areas PF and PFG, where neurons with mirror properties are found in the monkeys (see above). More complex is the situation for the frontal regions. A first issue concerns the location of the border between the two main sectors of the premotor cortex: the ventral premotor cortex (PMv) and the dorsal premotor cortex (PMd). In nonhuman primates the two sectors differ anatomically (Petrides & Pandya 1984, Tanné- Gariepy et al. 2002) and functionally (see Rizzolatti et al. 1998). Of them, PMv only has (direct or indirect) anatomical connections with the areas where there is visual coding of action made by others (PF/PFG and indirectly STS) and, thus, where there is the necessary information for the formation of mirror neurons (Rizzolatti & Matelli 2003). 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH MIRROR NEURONS 177 On the basis of embryological considerations, the border between human PMd and PMv should be located, approximately, at Z level 50 in Talairach coordinates (Rizzolatti & Arbib 1998, Rizzolatti et al. 2002). This location derives from the view that the superior frontal sulcus (plus the superior precentral sulcus) represents the human homologue of the superior branch of the monkey arcuate sulcus. Because the border of monkey PMv and PMd corresponds approximately to the caudal continuation of this branch, the analogous border should, in humans, lie slightly ventral to the superior frontal sulcus. The location of human frontal eye field (FEF) supports this hypothesis (Corbetta 1998, Kimming et al. 2001, Paus 1996, Petit et al.1996). In monkeys, FEF lies in the anterior bank of the arcuate sulcus, bordering posteriorly the sector of PMv where arm and head movements are represented (area F4). If one accepts the location of the border between PMv and PMd suggested above, FEF is located in a similar position in the two species. In both of them, the location is just anterior to the upper part of PMv and the lowest part of PMd. The other issue concerns IFG areas. There is a deeply rooted prejudice that these areas are radically different from those of the precentral gyrus and that they are exclusively related to speech (e.g., Grèzes & Decety 2001). This is not so. Already at the beginning of the last century, Campbell (1905) noted clear anatomical simi- larities between the areas of posterior IFG and those of the precentral gyrus. This author classed both the pars opercularis and the pars triangularis of IFG together with the precentral areas and referred to them collectively as the “intermediate pre- central” cortex. Modern comparative studies indicate that the pars opercularis of IFG (basically corresponding to area 44) is the human homologue of area F5 (Von Bonin & Bailey 1947, Petrides & Pandya 1997). Furthermore, from a functional perspective, clear evidence has been accumulating in recent years that human area 44, in addition to speech representation, contains (as does monkey area F5) a mo- tor representation of hand movements (Binkofski et al. 1999, Ehrsson et al. 2000, Gerardin et al. 2000, Iacoboni et al. 1999, Krams et al. 1998). Taken together, these data strongly suggest that human PMv is the homologue of monkey area F4, and human area 44 is the homologue of monkey area F5. The descending branch of the inferior precentral sulcus (homologue to the monkey inferior precentral dimple) should form the approximate border between the two areas (for individual vari- ations of location and extension area 44, see Amunts et al. 1999 and Tomaiuolo et al. 1999). If the homology just described is correct, one should expect that the observation of neck and proximal arm movements would activate predominantly PMv, whereas hand and mouth movements would activate area 44. Buccino et al. (2001) addressed this issue in an fMRI experiment. Normal volunteers were presented with video clips showing actions performed with the mouth, hand/arm, and foot/leg. Both transitive (actions directed toward an object) and intransitive actions were shown. Action observation was contrasted with the observation of a static face, hand, and foot (frozen pictures of the video clips), respectively. Observation of object-related mouth movements determined activation of the lower part of the precentral gyrus and of the pars opercularis of the inferior frontal 19 Jun 2004 14:34 AR AR217-NE27-07.tex AR217-NE27-07.sgm LaTeX2e(2002/01/18) P1: IKH 178 RIZZOLATTI � CRAIGHERO gyrus (IFG), bilaterally. In addition, two activation foci were found in the parietal lobe. One was located in the rostral part of the inferior parietal lobule (most likely area PF), whereas the other was located in the posterior part of the same lobule. The observation of intransitive actions activated the same premotor areas, but there was no parietal lobe activation. Observation of object-related hand/arm movements determined two areas of activation in the frontal lobe, one corresponding to the pars opercularis of IFG and the other located in the precentral gyrus. The latter activation was more … Consciousness and Cognition 22 (2013) 1152–1161 Contents lists available at SciVerse ScienceDirect Consciousness and Cognition j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / c o n c o g Mirror neurons and their function in cognitively understood empathy 1053-8100/$ - see front matter � 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.concog.2013.03.003 ⇑ Corresponding author. Fax: +39 02 72342280. E-mail addresses: [email protected] (A. Corradini), [email protected] (A. Antonietti). Antonella Corradini ⇑, Alessandro Antonietti Department of Psychology, Catholic University of the Sacred Heart, Largo Gemelli 1, 20123 Milano, Italy a r t i c l e i n f o a b s t r a c t Article history: Available online 11 April 2013 Keywords: Mirror neurons Empathy Reenactive empathy Rational explanation Social cognition Mindreading Theory–theory Simulation theory Emotion Intention understanding The current renewal of interest in empathy is closely connected to the recent neurobiologi- cal discovery of mirror neurons. Although the concept of empathy has been widely deployed, we shall focus upon one main psychological function it serves: enabling us to understand other peoples’ intentions. In this essay we will draw on neuroscientific, psycho- logical, and philosophical literature in order to investigate the relationships between mir- ror neurons and empathy as to intention understanding. Firstly, it will be explored whether mirror neurons are the neural basis of our empathic capacities: a vast array of empirical results appears to confirm this hypothesis. Secondly, the higher level capacity of reenactive empathy will be examined and the question will be addressed whether philosophical anal- ysis alone is able to provide a foundation for this more abstract level of empathy. The con- clusion will be drawn that both empirical evidence and philosophical analysis can jointly contribute to the clarification of the concept of empathy. � 2013 Elsevier Inc. All rights reserved. 1. Introduction The mirror neuron system (MNS) has been recently proposed as the biological basis of social cognition (e.g., Pineda, 2009). This encompasses a broad range of phenomena, which includes, among others, empathy (Gallese, Gernsbacher, Heyes, Hick- ok, & Iacoboni, 2011, Question 6). The term ‘‘empathy’’ is used to denote different phenomena (Roganti & Ricci Bitti, 2012). It is sometimes deployed to refer to simple forms of behavioural sharing, as occurs in emotional contagion: when a person is performing an action which is usually associated with the experience of a given emotion, another displays the same behav- iour (de Vignemont & Singer, 2006). This is the case of a baby who begins crying because another baby close to her is crying or the case of laughter which spreads in a group even though people are not aware of why the others are laughing. On the other hand, empathy can be conceived of as a mainly cognitive phenomenon, which allows us to figure out the propositional attitudes that are at the basis of another’s deciding, planning, and acting. Emotional aspects are not excluded, but they play a minor role in the empathic process. In the light of this special issue’s topic, empathy can be conceived of as a person’s capacity to understand what others intend to do by experiencing the sensations, emotions, feelings, thoughts, beliefs, and desires which the other is experiencing (or has previously experienced). The assumption is that, if we experience the mental states of a fellow person, we can under- stand her reasons for her acting in a given way, and thus understand the intentions underlying her behaviour. For instance, if we realise, by watching Tom, that he has been offended by Dick and that he is now becoming angrier and angrier as a con- sequence of such an offence, we can understand why Tom behaves aggressively towards Dick. In turn, the comprehension of another’s mental states is based, beside verbal communication, on the overt behaviour displayed by her (Avenanti & Aglioti, http://crossmark.crossref.org/dialog/?doi=10.1016/j.concog.2013.03.003&domain=pdf http://dx.doi.org/10.1016/j.concog.2013.03.003 mailto:[email protected] mailto:[email protected] http://dx.doi.org/10.1016/j.concog.2013.03.003 http://www.sciencedirect.com/science/journal/10538100 http://www.elsevier.com/locate/concog A. Corradini, A. Antonietti / Consciousness and Cognition 22 (2013) 1152–1161 1153 2006), thus the observation of others’ bodily signals can be an important source of intention ascription. For instance, as sug- gested by Wolpert, Doya, and Kawato (2003), facial expressions – one of the main body signals we use to communicate, intentionally or incidentally, our emotional state to the others – can be seen as actions aimed at revealing the subject’s intentions. The function of empathy in understanding others’ intentions can be analysed both from a scientific and a philosophical point of view. The aim of this essay is to address this topic from both perspectives. From the viewpoint of scientific inquiry, the distinction between different forms of detecting others’ intentions is taken into account by referring to recent psycho- logical literature. This will allow us to identify the specific form of empathy which is allegedly associated with MNS. Then, empirical data supporting the role of MNS in empathy will be shortly reviewed. The first section of the essay will end with some critical remarks about the need for conceptual clarification when appealing to MNS to ground empathy. These com- ments, by stressing the necessity of a fine-tuned analysis of such conceptual issues, will build the bridge to the philosophical section. This mainly focuses on whether reenactive empathy, that is to say cognitively understood empathy, can be con- ceived of as a genuine epistemic capacity, able to justify rational explanation. After a short introduction to the topic of empa- thy in contemporary social sciences, part 3.2. will be devoted to a defence of the soundness of rational explanation against criticisms raised by Hempel and other authors belonging to the empiricist tradition. In part 3.3, then, two arguments will be subjected to scrutiny, whose aim is to show that only reenactive empathy is able to ensure the validity of rational explana- tion. The upshot will be that neither argument proves to be conclusive. This result, however, does not definitively rule out empathy as an original kind of knowledge, since empirical evidence based on mirror neurons might offer some support to this epistemological thesis, in particular if basic kinds of empathy are taken into consideration. 2. Empathy and MNS from the point of view of psychology and neuroscience 2.1. Mirroring and mentalising mechanisms underlying empathy Empathy is a complex phenomenon involving different aspects and dimensions. In fact, the understanding of others’ intentions through the experience of their mental states may be underwritten by different processes. On the one hand, as shown by the example reported in the previous section, we can immediately understand the reasons for Tom’s aggressive behaviour on the basis of the perception of his face and/or the tone of his voice. We establish a direct connection between what Tom looks like (in terms of bodily appearance and bodily movements), his mental states, and his acts. On the other hand, we can understand Tom’s intentions by integrating the perceptual information Tom provides us with and some infer- ences based on contextual cues (for instance, the presence of other people on the scene who are mocking him), specific no- tions we have about Tom (for instance, remembering that Tom is a choleric guy), and abstract concepts (for instance, our conviction that an offended man should always take revenge). In the fields of psychology and the neurosciences some distinctions have been drawn in the attempt to clarify the mech- anisms underlying the understanding of others’ intentions. A relevant starting point may be the distinction which has been made, under different concepts and linguistic labels, between a system which allows human beings to comprehend imme- diately others’ intentions and a system which allows humans to reach such an outcome through an inferential process which implies the mediating role of some forms of reasoning. This distinction relies on a more fundamental distinction which has been recurrently proposed by different authors in recent years in the domain of thinking and decision-making processes (Sloman, 1996), namely, the distinction between the so-called System 1 and System 2. System 1 (Stanovich & West, 2000) – also labelled as intuitive (Pretz, 2008), experien- tial (Slovic, Finucane, Peters, & MacGregor, 2002), tacit (Hogarth, 2001), impression-based (Kahneman, 2003) – is fast and action-oriented; it is activated unintentionally and its functioning is rigid and partially behind the control of the individual. Usually it operates effortlessly on the basis of associations. System 2 (Stanovich & West, 2000) – also called analytical (Slovic et al., 2002), deliberative (Hogarth, 2001), judgment-based (Kahneman, 2003), rational (Epstein, 1994) – operates slowly, intentionally, and flexibly, predominantly on the basis of abstract representations and logical rules. Usually it is not emotion- ally charged. The functioning of System 2 may fail to be optimal because of the excessive cognitive load it requires, its slow- ness, and the large amount of effort its activation needs. In this vein, with specific reference to social cognition, Bohl and van den Bos (2012) proposed the distinction between Type 1 and Type 2 process. The former is fast, efficient, stimulus-driven, and lacks flexibility. The latter is slow, involves a high cog- nitive load and elaboration, is flexible and accessible to consciousness. With a more specific focus on processes involved in understanding other people’s intentions, Waytz and Mitchell (2011) distinguished between mirroring and self-projection mechanisms. The first mechanism enables us to understand other people by experiencing vicariously their mental states: thanks to such a mechanism, the others’ mental states are mirrored in our mind. Through the second mechanism we project our mental states onto the situation of another individual, so to infer her mental states. According to the authors, the two mechanisms involve different degrees of immediacy in others’ understanding. Mirroring is a sort of on-line process which al- lows us to resonate immediately according to what another person is experiencing; self-projection, by contrast, implies imag- ining off-line what we should experience if we were in the other’s shoes and then attributing such an experience to her. The distinction between mirroring and self-projection overlaps partially the distinction between mirroring and mentalis- ing (Chiavarino, Apperly, & Humphreys, 2012). The mirroring system responds to observation of others’ acts and seems to 1154 A. Corradini, A. Antonietti / Consciousness and Cognition 22 (2013) 1152–1161 code their goals immediately by establishing purely behavioural relations between the perceptual appearance of the actor and her corresponding intentions. Mentalising instead requires inferences about the mental states which are at the basis of the behavioural relations. More precisely, the second system has two subcomponents: a representational one, which serves the task to represent the actor’s intention as a mental state (but not as a behavioural relation), and a conceptual com- ponent ‘‘representing the semantic and logical properties of intentions, abstractly reasoning over these properties, and relat- ing them to other mental states’’ (Chiavarino et al., 2012, p. 286). 2.2. Mirror neurons and empathy: empirical data The neural circuits constituting MNS have been proposed as the best candidate for the biological basis of empathy, which is to be thought of as the expression of the mirroring process. In fact, MNS has been invoked as a putative interpretation of empathy and some experimental findings have been taken as evidence supporting the involvement of MNS in empathy (Gal- lese, 2001, 2003; Iacoboni, 2009; Preston & de Waal, 2002). First of all, it is documented that humans, when watching people showing facial expressions corresponding to well-de- fined emotions, covertly activate the same muscles which are involved in the creation of those expressions (Dimberg, Thun- berg, & Elmehed, 2000). Moreover, if people are prevented from automatically imitating the muscle contractions of the faces they are exposed to (for instance, by compelling them to keep a pencil with the teeth transversal to the mouth), they become less able to detect the emotional expression of the observed faces (Niedenthal, Barsalou, Winkielman, Krauth-Gruber, & Ric, 2005). This experimental finding supports analogous results observed in patients affected by the Moebius syndrome, which impedes them to move their facial muscles: as a consequence of such an impairment, these patients fail to recognise the emotions expressed by others (Cole, 2001). Finally, it is worth noting that the same cortical areas are activated when people observe and imitate faces expressing emotions (Leslie, Johnson-Frey, & Grafton, 2004). Hence, it is proved that, in emotion recognition, observation and action are linked together, as in the case of the functional actions directed at manipulating things, which have been the main topic of investigation in MNS field. These findings, however, only concern emotion recognition, which is not empathy, but rather its precursor or precondi- tion. Further empirical evidence is required. Indeed, other studies showed that the link between observation and perception also regards empathy. For instance, if individuals are paired with a confederate who imitates their postures, gestures, and body movements during the execution of a joint task, they perceive the confederate as more agreeable than controls paired to a non-imitating confederate do (Chartrand & Bargh, 1999). In addition, individuals who spontaneously imitated the behaviour of the confederate scored higher on an empathy scale subsequently, showing a positive relation between the fre- quency of imitative behaviours and the empathy rates (Chartrand & Bargh, 1999). Two emotional reactions have been often investigated in the attempt to prove the involvement of MNS in empathy: pain and disgust. As to pain, Avenanti, Bueti, Galati, and Aglioti (2005) recorded the excitability of the muscle of the hand which generates an approaching movement toward a noxious stimulus (a needle): when people looked at a video showing other people whose hand was penetrated by a needle in the same point, the excitability of the muscle decreased (as if they were trying to move away the hand from the needle); in addition, the reduction of the excitability of the muscle was proportional to the estimated level of pain the subjects attributed to other people when their hand was penetrated by the needle (see also Avenanti, Minio-Paluello, Sforza, & Aglioti, 2009; Valeriani et al., 2008). As far as the brain counterparts of pain experience are concerned, it was showed that neurons in the anterior cingulate cortex responding to painful stimuli applied to the subject’s hand also fired when the subject observed another person being stimulated by the same noxious stimuli (Hutchison, Davis, Lozano, Tasker, & Dostrovsky, 1999). Anterior cingulate cortex, together with some regions of the insula, was also activated by observing relatives who were not currently exposed to pain- ful stimuli, but would be stimulated painfully later (Singer et al., 2004). Hence, not only the direct observation of suffering people, but also the prefiguration of a future pain affecting others activate the brain areas corresponding to the actual expe- rience of pain in first person. The same message is provided by studies concerning the neural counterparts of disgust. It has been proved that the same brain structure (the insula, in this case), which is active when the individual experiences disgust personally, is activated even when the individual looks at faces expressing disgust and that the intensity of such an activation is proportional to the level of disgust expressed by the face (Phillips et al., 1997). The evidence was later supported by recording the activity of neurons in the anterior part of the insula through electrodes implanted in the brain of epileptic patients (Krolak-Salmon et al., 2003). A clear proof that the same neural counterparts are involved in experiencing disgust and observing other people experienc- ing that emotion was provided by Wicker et al. (2003) in a fMRI study where the same participants were both exposed to disgusting odours and to pictures of persons smelling the same odours. The impairment in experiencing negative emotions is associated with the impairment of recognising similar emotions in other people. In fact, a case was reported of a patient with brain lesions in the putamen and in the insula who failed to sub- jectively experience disgust (and, as a consequence, to react to disgusting situations appropriately) and also was not able to detect disgust in other people by observing their facial expressions or by listening to non-verbal sounds which they pro- duced, as well as to the prosodic aspects of their speech (Calder, Keane, Manes, Antoun, & Young, 2000). A similar case was successively reported by Adolphs, Tranel, and Damasio (2003). When trying to find evidence that MNS is specifically involved in empathy, we can point to the fact that the activation of brain areas included in MNS has been recorded in participants both when they were simply looking at actors showing facial A. Corradini, A. Antonietti / Consciousness and Cognition 22 (2013) 1152–1161 1155 expressions whose emotional meaning corresponded to that of the story they were telling (Decety & Chaminade, 2003) and when they were asked to identify the emotional states of actors by observing their body postures, gestures, and facial expres- sions (Lawrence et al., 2006). Further support came from the experiment executed by Schulte-Rüther, Markowitsch, Fink, and Piefke (2007): mirror-neuron mechanisms were activated when participants, exposed to facial expressions, had to identify both the emotions concurrently experienced by themselves and the emotions expressed by the others’ faces. The involvement of MNS in empathy is also proved by correlational studies. Two investigations demonstrated that the level of emotional empathy developed by the participants was correlated to the intensity of the activity of premotor areas, presumably containing mirror neurons, when the participants were asked to look at other people carrying out the act of grasping with different intentions, as suggested by contextual hints (Kaplan & Iacoboni, 2006) or to listen to sounds pro- duced by human actions (Gazzola, Aziz-Zadeh, & Keysers, 2006). More specifically, participants who showed higher activa- tion of brain areas involved in MNS when looking at facial expressions by focussing on their emotional valence (Schulte- Rüther et al., 2007) obtained high scores on empathy scales. MNS, together with other brain structures such as the limbic system and the insula, constitutes a large neural circuitry which has been proved to be activated by both the execution, through imitation, and observation of facial expressions asso- ciated to emotional experiences (Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003; Iacoboni & Lenzi, 2002). The association between MNS and both the subjective experience of emotions and the detection of the same emotions in others through the observation of their behaviour is further supported by a fMRI study which showed that the activation of MNS in preadoles- cents while observing and imitating emotional facial expressions is positively correlated with the level of empathic skills (Pfeiffer, Iacoboni, Mazziotta, & Dapretto, 2008). An additional support is provided by clinical studies carried out with people affected by autism. On the one hand these patients – who are impaired in recognising emotions from others’ facial expres- sions and to imitate such expressions – fail to show the usual reactions when looking at other people being affected by pain- ful stimuli (Minio-Paluello, Baron-Cohen, Avenanti, Walsh, & Aglioti, 2009). On the other hand people with autism show deficits in MNS functioning and their level of activity of MNS is reduced in correspondence with the level of severity of the pathology (Dapretto et al., 2006). 2.3. Mirror neurons and empathy: conceptual problems One of the main messages which are associated to the findings concerning the involvement of MNS in the understanding of others’ mental states, including intentions, is that such an understanding does not exclusively depend on linguistic and mentalistic processes (Gallese, 2001, p. 34). On the contrary, intentions are embodied. Such an embodiment is shared both by the actor and the observer and relies on the motor schema of action. When the motor schema of the actor matches a mo- tor schema in the repertoire of the observer, the intended meaning of the action is detected (Gallese, 2001, p. 36). If this gen- eral framework is applied to empathy, the consequence is that empathy is grounded in the experience of the lived body: others are conceived ‘‘not as bodies endowed with a mind but as persons like us’’ (Gallese, 2001, p. 43). In this way we can recognise why persons behave in a certain manner. In some circumstances, the comprehension of the intentions of others’ behaviour occurs predominantly on the basis of the emotions they are experiencing rather than of the functions of the actions they are performing. When this happens, empirical findings summarised above suggest that MNS is involved, either because some cerebral areas belonging to MNS are directly activated or because other brain structures, connected to the main mirror-neuron areas, are activated, such that they successively involve the proper mirror-neuron areas. In any case, the resulting outcome is that the same brain struc- tures, which are activated when we experience the affective state the other is experiencing, are activated. This would lead the affective states of other people to resonate in the mind of the perceiver (Gallese, 2001, p. 38; Rizzolatti & Sinigaglia, 2006, p. 121) or, put differently, would generate in the perceiver a sort of inner imitation of what the other is feeling (Iacoboni, 2008, chap. 4). Another way of thinking of this is that the cerebral system of the observer would be activated as if she were behaving as the observed human being. This occurs because the observed behaviour is translated into a program which acts as a sort of signal (efference copy signal) which enables the simulation of the behaviour (Gallese, 2001, pp. 40–41). As a con- sequence, the other’s behaviour is modelled as an action thanks to the behavioural equivalence between the perceiver’s and the other’s actions (Gallese, 2001, p. 39). A first critical remark is that further clarification of the mental process supported by MNS during an empathic relation is required. Resonance, inner imitation, simulation, and modelling are different processes and the authors claiming that MNS grounds empathy should be more explicit and precise about the psychological counter- parts of the corresponding cerebral activations. Whatever these processes may be which are supported by MNS and lead to empathy, authors maintaining that MNS is involved in empathy generally agree that intention understanding does not involve any form of abstract thought. To put it in the authors’ words, it is ‘‘non-predicative’’ (Gallese, 2001, p. 44), ‘‘without verbal mediation’’ (Rizzolatti & Sinigaglia, 2006, p. 120), ‘‘without the need of theorising’’ (Gallese, 2001, p. 41), ‘‘without propositional attitudes’’ (Gallese, 2001, p. 41), ‘‘non-inferential’’ (Gallese, 2001, p. 44; Rizzolatti & Sinigaglia, 2006, p. 174), ‘‘without any knowledge operation’’ (Riz- zolatti & Sinigaglia, 2006, p. 127), ‘‘not needing cognitive processes’’ (Rizzolatti & Sinigaglia, 2006, p. 174), ‘‘pre-reflective’’ (Iacoboni, 2009, p. 666). In these authors’ view, MNS leads us to comprehend others’ experience in the absence of any con- ceptual representation and inference. Now, how should this form of understanding be conceived? This is a list of the adjec- tives which are attributed to it: ‘‘direct’’ (Gallese, 2001, p. 41), ‘‘immediate’’ (Gallese, 2001, p. 41; Rizzolatti & Sinigaglia, 2006, p. 127), ‘‘effortless’’ (Iacoboni, 2009, p. 666), ‘‘automatic’’ (Gallese, 2001, p. 41; Iacoboni, 2009, p. 666), ‘‘implicit’’ (Gal- 1156 A. Corradini, A. Antonietti / Consciousness and Cognition 22 (2013) 1152–1161 lese, 2001, p. 41), ‘‘unconscious’’ (Gallese, 2001, p. 41), ‘‘subpersonal’’ (Gallese, 2001, p. 42 and 46). Here, too more precision seems to be required (Debes, 2009). In fact these attributes have different meanings and do not implicate one another. For instance, pure knowledge operations and cognitive processes, with no form of embodiment, can also be immediate and effortless, if adequately trained. Also the meaning of ‘‘automatic’’ and ‘‘unconscious’’ should be specified. A process can be automatic by its very nature or because it has become such after having been carried out for a long time with effort and the labour of reasoning. The same is true of the unconscious character of intention understanding: is it a process which has become unconscious as a consequence of its automatisation or because it has always been unconscious? In other words: the process might be conscious (and involving effort) when the individual is trying to learn to carry it out, but it becomes unconscious (and effortless) when she had learnt to master it. In addition: does the unconscious character of the process make reference to how the process develops or to the outcome of the process? We can be unaware of how we compute the sum 5 + 2, but we are aware of the output of the process (and also of the fact that we are computing the sum). Also the claim that intention understanding supported by MNS through empathy fails to involve knowledge and cognitive mech- anisms can be questioned. As noted by Roganti and Ricci Bitti (2012, pp. 583–584), appraisal processes are always implied in emotion comprehension, and thus an interpretative component can never be discarded, otherwise only a form of emotional synchronisation or synthonisation, but not a real understanding, occurs. Thus, the specific forms of cognition which should be excluded by the kind of empathy supported by MNS have to be clarified, since it has been proved that other cortical re- gions, beside MNS, are involved in cognitive manifestations of empathy (Shamay-Tsoory, Aharon-Peretz, & Perry, 2008). In conclusion, it appears that a more fine-grained analysis of the features of the empathic relation supported by MNR is needed. To this end, this issue has to be addressed from the philosophical perspective, which we turn to now. 3. From mirror neurons to reenactive empathy 3.1. Empathy as reenactive empathy As the first part of this essay has shown, the renewed, current interest in empathy is strictly related to empirical research in the fields of neurobiology and psychology. In particular, the discovery of MNS in monkeys has given new impulse to the scientific treatment of empathy. However, the notion of empathy has a long philosophical tradition, characterised by many ramifications and several divergent approaches (for an informed reconstruction of the history of empathy see Stüber, 2006, Introduction, and 2008). As far as philosophy of the social sciences is concerned, the most influential twentieth century sup- porter of empathy has been the philosopher of history Robert Collingwood (1949) who, against explanatory monism, main- tained that explanation in history requires an essential empathic component. In fact, we cannot explain the behaviour of a historical character without re-enacting her intentions, beliefs, desires and choices. Yet, the role of reenactive empathy has not always been positively evaluated within the philosophy of the social sciences, partly because it introduces a sharp dual- ism between natural and social sciences, partly because it appears to represent a capitulation to any sort of subjectivism and arbitrariness (see Popper’s criticism of the epistemological role of empathy in Popper, 1972, 4.12). In recent years, however, authors such as Jane Heal and Karsten Stüber have revived the fortunes of empathy and have argued in favour of a strict correlation …