STUDENT PSYCHOLOGY JOURNAL VOLUME II

MIRROR NEURONS: OUR CURRENT UNDERSTANDING

Georgina Mullen Senior Freshman, Psychology, UCD [email protected]

ABSTRACT Mirror neurons are a relatively new phenomena, first observed in the premotor cortex of macaque monkeys when a number of neurons were observed to respond both when a monkey performed a goal orientated task, and when the monkey watched another (human or monkey) perform that task. A number of researchers have suggested that mirror neurons also exist in humans. It is proposed that a human mirror neuron system may contribute to a number of cognitive functions such as action understanding; ‘theory of mind’, humans’ abilities to infer another’s mental state through experiences or others’ behaviour; emotion understanding; imitation; and speech perception. Faulty human mirror neurons have even been suggested to underpin social impairments such as those characteristic of Autistic Spectrum Disorder (ASD). However, there has been much debate regarding the existence and functional roles of mirror neurons in humans. While there is much literature regarding human mirror neurons, the majority consist of reviews while few concern empirical experiments. Additionally concern has been expressed for some of the experimental methods used in empirical studies. A recent experiment from Mukamel et al. (2010) is the first of its kind to directly gather evidence for the existence of mirror neurons in humans and for their function subserving action understanding. The present review critically outlines the growth in this controversial field of research, taking into account the recent direct recording of human mirror neurons, and what implications this may have on our understanding of social cognition.

INTRODUCTION Social cognition involves any process among conspecifics, allowing for individuals to understand the actions, intentions and emotions of others. Such social abilities are a crucial aspect of human survival and success (Blakemore et al., 2004). For this reason much research has been devoted to exploring what mechanisms and processes underlie social cognition.

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This expansive research has resulted in what has been suggested by some to be the greatest recent discovery in neuroscience; mirror neurons (Ramachandran, 2000). Ramachandran (2000) suggests that the discovery of mirror neurons will impact the field of psychology as DNA influenced biology; that mirror neurons can provide a unifying framework which can explain a number of humans’ mental abilities. However, such grand claims have not gone undisputed. While it is largely accepted that mirror neurons exist in macaque monkeys where they were originally recorded (Casile et al., 2011), researchers have been skeptical regarding the existence and proposed functions of a human mirror neuron system (Dinstein et al., 2008).

MIRROR NEURONS IN MONKEYS Direct recordings in macaque monkeys have found that both observation of an action and performance of that action can lead to the discharge of a subset of neurons, called mirror neurons (Gallese et al., 1996). These mirror neurons were first observed in the F5 area of the premotor cortex (di Pelegrino et al., 1992; Gallese et al., 1996) but were later observed in the inferior parietal lobule (Fogassi et al., 2005; Rozzi et al., 2008) (see Figure 1). Further research investigated mirror neuron activity in two conditions; when a monkey watched a human hand reach and grasp an object (the visible condition), and when the monkey watched a human hand reach and then disappear behind a screen (the hidden condition) (Umilta et al., 2001). Some mirror neuron activation was recorded during the hidden condition, but only when the monkeys had first seen an object at the location behind the screen, suggesting that mirror neurons in monkeys are responsible for action understanding (Umilta et al., 2001). Furthermore Fogassi et al. (2005) suggested that mirror neurons contribute to monkeys’ understanding of intention, based on their experiment in which different populations of parietal neurons fired when a monkey grasped an object which was subsequently eaten, and when the monkey grasped an object which was subsequently placed in a box.

A HUMAN MIRROR NEURON MECHANISM Based on the discovery of mirror neurons in monkeys, researchers began to question whether a similar mirror mechanism may exist in humans (Gallese et al., 1996). Experiments that support the existence of a human

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mirror neuron mechanism have mostly used indirect methods which indicate neural activation. Some of the first evidence was derived from Hari et al.’s (1998) study which recorded neuromagnetic oscillatory activity in participants’ precentral cortex. Hari et al. (1998) measured brain activity using magnetic resonance imaging (MRI) and magnetoencephalography (MEG) while participants manipulated a small object with their hand. They observed a significant modification in neuromagnetic activity when participants’ observed others manipulating objects. This indicated the existence of an action observation/execution matching system in the human brain, similar to the one previously observed in monkeys (Hari et al., 1998). Subsequently a number of empirical studies investigated the presence and possible functions of a human mirror system. These appeared to support a mirroring mechanism within humans located in the frontal and parietal areas of the brain (Iacoboni et al., 1999; Iacoboni et al., 2005), and in other motor regions (Hari et al., 1998; Koski et al., 2003; Gazzola & Keysers, 2009) (see Figure 2). Additionally multisensory mirroring mechanisms have been observed in nonmotor regions such as the amygdala and insula (Hutchison et al., 1999; Calder et al., 2000; Wicker et al., 2003; Keysers et al., 2004). These studies used a number of techniques to measure brain activation, including functional (f)MRI, MEG, electroencephalography (EEG), positron emission tomography (PET), transcranial magnetic stimulation (TMS), and lesion studies (observation of neurological patients). These methods do not allow for a direct and exclusive measure of mirror neuron activity, which has led a number of researchers to question the validity of the assumption that a mirror neuron system exists in humans (Dinstein et al., 2008; Hikock, 2009). While it is clear that these indirect methods cannot provide definite evidence, they are thought to correlate well with direct measures (Iacoboni, 2009). Dinstein et al. (2008) caution the inferences drawn from indirect methods such as fMRI as responses may not be generated by mirror neurons but by other neural populations. These interpretations therefore fail to take into account the fact that mirror neurons in monkeys only make up a small minority of neurons in these areas and thus the activation may not be from mirror neurons but rather from neighbouring visual, motor, and visuomotor neurons (Dinstein et al., 2008). Recent research from Mukamel et al. (2010) recorded single neuron activity in humans, rather than using indirect methods. This recording

REVIEW during action observation and execution appears to support previous indirect suggestion that a mirroring mechanism exists in humans. While past research has focused on recording activity in areas of the brain homologous to regions containing mirror neurons in monkeys, Mukamel et al. (2010) detected a mirroring mechanism in areas of the medial frontal and temporal cortices which were not previously suggested to contain mirror neurons. Mukamel et al. (2010) did not record in areas where human mirror neurons had been suggested as placement of electrodes was determined only by clinical considerations (participants consisted of patients with pharmacologically intractable epilepsy). Despite Mukamel et al.’s (2010) influential evidence, some criticisms of a human mirroring mechanism remain valid. For example, the argument that evidence for mirror activation in humans does not have key features in common with the mirror neuron system seen in monkeys (Heyes, 2009). Specifically, human mirror activation occurs in both homologous areas and in areas where mirror neurons have not been reported in monkeys (Dinstein et al., 2008). Additionally the majority of mirror neurons found in monkeys are responsive to actions on objects, while proposed human mirror neurons often respond to gestures as well as actions on objects (Hickok, 2009).

POTENTIAL FUNCTIONS OF A HUMAN MIRROR MECHANISM

ACTION UNDERSTANDING As mirror neurons in monkeys are thought to be the neural basis of action understanding (Umilta et al., 2001), when researchers began to question the existence mirror neurons in humans, they did so with the assumption that if mirror neurons were observed, their function would involve action perception (Hari et al., 1998; Grezes & Decety, 2001; Gazzola & Keysers, 2009; Mukamel et al., 2010). Further research questioned what other functions mirror neurons might subserve, including higher social cognitive abilities such as communication (Rizzolatti & Craighero, 2004), empathy (Iacoboni, 2009), sensations (Keysers et al., 2004) and emotions (Wicker et al., 2003). Gazzola and Keysers (2009) used fMRI to record shared neural activity in individuals during action observation and execution. The areas of the brain suggested to contain shared voxels include the dorsal premotor cortex, the supplementary and cingulate motor areas, the superior parietal lobe, the somatosensory cortices and the cerebellum (Gazzola & Keysers, 2009) (see Figure 2). While Gazzola and Keysers

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(2009) propose that their findings contribute to the body of evidence that supports a human mirror neuron system, they do caution that further research must be carried out as a voxel contains millions of neurons. Stronger evidence from Mukamel et al.’s (2010) report suggests that multiple systems in humans may have neural mirroring mechanisms for both the integration and differentiation of execution and observation of actions, supporting earlier indirect evidence. Some recent reviews have argued that most of the current findings offer little more than a minor, non-specialised contribution to action understanding, rather than a major specialised one (Heyes, 2010; Hikock, 2009). It has been argued that this weakens the theory behind a human mirror neuron system (Hikock, 2009). However, Heyes (2009) suggests that this criticism against a human mirror mechanism is only valid if mirror neurons are accepted to have evolved for the adaption of action understanding. For this reason Heyes (2009) champions the alternative suggestion that mirror neurons are a byproduct of associative learning.

IMITATION AND EMPATHY A human mirror neuron mechanism has been suggested to mediate imitation. While this assumption is widely accepted there is little empirical evidence for mirror neurons’ role in imitation. (Catmur et al., 2009). Mukamel et al. (2010) observed an opposing pattern of excitation and inhibition when recording single cell activity during action observation and execution which they suggested may contribute to an individual’s sense of being the owner of their action, but may also exert control on unwanted imitation during observation. Earlier studies also support this proposition, such as Iacoboni et al.’s (1999) fMRI experiment in which two areas of the brain; the inferior frontal gyrus and the rostral part of the posterior parietal cortex showed activation both during imitation and observation. In addition studies of neuropsychological patients have offered evidence which suggests a role for mirror neurons in imitation, although they cannot offer specific locations of mirror neurons (Catmur et al., 2010). For example, lesions to the inferior parietal lobe (an area thought to contain mirror neurons) often results in apraxia, a deficit in imitation and mimicking (Wheaton & Hallett, 2007). Goldenberg and Karnath (2006) also reported impaired imitation, specifically in hand gestures after lesions to the left inferior parietal lobe. Accounts of echopraxia, a condition in which patients suffering from frontal lobe

REVIEW damage repeat all observed movements (Luria, 1966), and ‘obstinant imitation behaviour’, a severely increased urge to imitate observed action, even when explicitly instructed not to (Lhermitte et al., 1986) support a mirror neuron function for imitation as both conditions involve frontal lobe damage and increased imitation (Bien et al., 2009). Furthermore Iacoboni (2005) suggests that a core cortical circuitry exists for imitation, and that this system’s interaction with the limbic system allows individuals the ability for social mirroring and empathy. Carr et al. (2003) propose that empathy is enabled by a large-scale neural network composed of the mirror neuron system connected by the insula to the limbic system. In such a system mirror neurons would support the simulation of facial expressions observed in others, which would then activate the limbic system, allowing the observer to experience others’ emotions (Carr et al., 2003). Further research has used fMRI study on typically developing preadolescents asked to observe and imitate emotional expressions, and has found that activity in mirror neuron areas is positively correlated with interpersonal competence and empathetic concern (Pfeifer et al., 2008).

EMOTIONS AND SENSATION Higher social cognitive functions such as understanding others’ emotions and sensations have also been attributed to a neural mirroring mechanism (Hutchison et al., 1999). Wicker et al. (2003) conducted a study using fMRI when participants both inhaled odours that induced a strong feeling of disgust, and observed others’ emotional expressions of disgust. Wicker et al.’s (2003) findings suggested that observing an emotion activates a similar neural representation of that emotion. Keysers et al. (2004) questioned whether watching a movie that depicts touch would activate the viewer’s somatosensory cortices and found that while the primary somatosensory cortex was not activated, the secondary somatosensory cortex was, indicating that the neural mechanisms which subserve the sensation of touch may also be the basis of humans’ understanding of touch. While such studies suggest that mirror-like neurons may exist for emotions and sensations, without direct single cell recording, this suggestion remains tentative.

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SOCIAL IMPAIRMENTS Because of the large number of social cognitive functions that have been associated with human mirror neurons, researchers have proposed that a dysfunction of the mirror neuron system may result in symptoms of social impairment, particularly those typical of ASD (Ramachandran & Oberman, 2006). ASD is characterised by abnormal social development, poor language capacity, difficulty mimicking others’ actions and strong obsessional interests from a young age. Many of these have been associated, albeit weakly, with mirror neurons (Fan et al., 2010). Conflicting evidence exists regarding mirror neurons’ potential contribution to ASD, and what little empirical evidence exists is indirect (Fan et al., 2010). Oberman et al.’s (2005) study suggests that mirror neurons appear faulty in those with ASD. However, further study has indicated that mirror neuron function appears to be retained to some degree in individuals with ASD (Hamilton et al., 2007; Fan et al., 2010). Ultimately, further research into the neurocognitive models of social behaviour both within and beyond the dysfunctional mirror neuron account is necessary (Fan et al., 2010).

CONCLUSION Evidently this controversial field of research has greatly evolved in the past decade. Researchers have been critical of some of the inferences made regarding mirror neurons and higher cognitive functions, which are often based on little empirical evidence but largely based on assumptions (Hikock, 2009). Due to these inferences, some have become skeptical of the existence of a human mirror neuron system. Currently, evidence suggests that mirror neurons do exist in animals. However, implications that mirror neurons play a causal role in cognitive functions such as ‘theory of mind’ (Gallese & Goldman, 1998), empathy (Carr et al., 2003), sensations (Hutchison et al., 1999), language (Rizzolatti & Craighero, 2004) and autism (Oberman et al., 2005) are weak and are far from being widely accepted by researchers. These proposed connections between mirror neurons and social functioning is in no doubt fascinating, and may greatly expand our current understanding of the human brain. Without repeated, sound empirical evidence, the suggestion that human mirror neurons cause social cognitive functions remains speculative. Further knowledge of mirror neurons can also be gained through understanding their evolution (Heyes, 2009). Mirror neurons can offer further insight into

REVIEW the social brain, but to achieve this, speculation and controversy must be replaced by careful experimentation in order to reach a solid scientific understanding.

Figure 1. Lateral view of the left hemisphere of the macaque brain. Highlighted areas contain neurons that discharge during both observation and exectuion of bodily movements (created from data recorded by Gallese et al., 1996, and Rozzi et al., 2008).

Figure 2. Lateral view of the left hemisphere of the human brain. Highlighted areas indicate regions in which voxels are shared between action observation and execution (created from data recorded by Gazzola and Keysers, 2009).

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