In the present study, we found that rTMS over the right IPL significantly impaired the subjects’ performance on discriminating self-faces from other-faces. Subjects’ responses included more false alarms (identifying an image containing mostly ‘other’ as ‘self’) after right IPL stimulation. Stimulation of a control site, the anatomically homologous region in the LH, produced no significant difference in performance. Thus, the right IPL appears to be an essential component of the neural network for visual self-other discrimination. The exact nature of the impairment, as seen in a heightened false alarm rate, can be interpreted either as subjects’ overinclusion of stimuli containing any elements of ‘self’ (i.e. less conservative ‘self’ criteria) or a more conservative strategy when responding to ‘other’. This finding is also in line with neuropsychological evidence for right parietal involvement in own-body awareness (Berlucchi and Aglioti, 1997
; Blanke et al
) and agency (Farrer and Frith, 2002
; Chaminade and Decety, 2002
We propose that self-recognition is one component of a system representing the self, and specialized in the RH. This system has two complementary roles. First, it may use a mirror neuron mechanism to establish shared representations between self and others to enable social communication and intersubjectivity (Gallese, 2003
). Second, it implements a mechanism to distinguish representation of the self from that of others, which is critical for maintaining an individual sense of unity and agency. The mirror neuron system occupies the IPL and inferior frontal cortex (Rizzolatti et al
; Gallese et al
; Fogassi et al
) and similar fronto-parietal networks are implicated in self–other discrimination (Decety and Sommerville, 2003
). Indeed, in our previous fMRI study, we reported that activity in a fronto-parietal network in the RH increases the more a face resembles the self (Uddin et al
). This RH network overlapped with mirror neuron areas previously identified by separate experiments in our lab (Iacoboni et al
). In line with this suggestion, a recent fMRI study shows that a dysfunction of the mirror neuron system may account for some of the social deficits in children with autism spectrum disorder (ASD) (Dapretto et al
). Indeed, the failure to develop a ‘theory of mind’ is prominent in autism (Frith and Happe, 1999
), i.e. a separate representation of self and others.
In humans, the mirror neuron system has been shown to be involved in action observation and imitation (Iacoboni et al
; Rizzolatti and Craighero, 2004
; Molnar-Szakacs et al
). It has also been found that children who have developed the ability to self-recognize are more likely to engage in synchronic imitation with other children (Asendorpf and Baudonniere, 1993
). Thus, it appears that there is a developmental link between self-recognition and imitation, which may in part be supported by the mirror neuron system. Furthermore, this link between self-recognition and social engagement through imitation may indicate that indeed the neural mechanisms of self–other discrimination and social interaction are at least in part overlapping. Although the present study cannot provide definitive proof that the behavioural effect reported here is due to a disruption of mirror neurons in the right IPL, we believe that this is a plausible explanation of our findings, as the previous imaging data that guided our stimulation site (Uddin et al
) overlap quite well with the inferior parietal mirror neuron area identified in previous experiments in our lab (Iacoboni et al
Mirror neurons are typically associated with action observation and dynamic visual stimuli, whereas subjects in our experiment watched static images of neutral faces. However, the activation of mirror neuron areas in response to static biological stimuli has been previously observed (Johnson-Frey et al
; Carr et al
; Dapretto et al
). Thus, a mirror neuron response to our stimuli is probable.
It is unlikely that a disruption in the neuronal pool of inferior parietal mirror neurons can account for the whole effect reported here. In fact, mirror neuron areas identified by previous fMRI studies tend to be quite bilateral (Iacoboni et al
; Molnar-Szakacs et al
), whereas the effect reported here is clearly lateralized to the RH. As discussed, the right IPL has often been associated with the implementation of self-awareness (Spence et al
) and body schema (Berlucchi and Aglioti, 1997
). It is likely that the essential role of the right IPL in self–other discrimination revealed by rTMS results from a combination of bilateral functional mechanisms implemented by mirror neurons and lateralized functional mechanisms associated with more general aspects of self-representation and body schema.
A possible concern is that the effect we report may not be specific to self-recognition, and may reflect disruption of processing in more general face discrimination tasks. Due to practical constraints in stimulation procedures that make it difficult to run multiple tasks in multiple cortical areas, we did not run a control task condition in which subjects had to discriminate other non-self familiar faces. However, we believe it highly unlikely that our result would be seen for a general face discrimination task, as most neuroimaging studies of general face discrimination show activity in superior temporal gyrus and fusiform gyrus (Andrews and Ewbank, 2004
; Grill-Spector et al
). Conversely, our stimulation site was guided by previous imaging data that demonstrated right IPL activation during self-face recognition (Uddin et al
It is known that rTMS stimulation to a given brain region has both local and potentially interhemispheric effects. For this reason, we included as a control stimulation condition the homologous cortical region of the LH (left IPL). Though it is possible that some of the effects on behaviour we see after right IPL stimulation may result from alteration of activity in regions highly interconnected to this area, the effect of stimulation should be strongest on the targeted site and relatively much weaker at transcallosal sites. One target of particular interest to this study is the right inferior frontal gyrus, the other component of the fronto-parietal system responsive to self-faces. Assessing the effects on behaviour of targeting this region with rTMS is a direction for future research.
Another possible control condition is that of sham TMS. Though sham stimulation may be used as a possible control, there is still much unresolved debate about the validity of sham stimulation. In a systematic study designed to assess the validity of sham stimulation, Loo and colleagues (2000
) found that ‘none of the coil positions studies met the criteria for an ideal sham’. Furthermore, Lisanby and colleagues (2001
) found that some sham TMS conditions produce substantial cortical stimulation, casting further doubt on the validity of this control. Additionally, it is often obvious to the subject that he/she is receiving no actual stimulation. Therefore, we chose an active stimulation condition as a control by using the anatomically homologous site in the LH.
In conclusion, we show for the first time that disruption of processing in the right IPL is sufficient to degrade self-face recognition performance, suggesting a causal role for this region in self–other discrimination. This is the first evidence demonstrating that a human brain area is necessary for the discrimination of the self-face from other familiar faces, a correlate of maintaining a distinct representation of self while engaging with others.