The Role of the Right Temporoparietal Junction in Intersensory Conxict: Detection Or Resolution?
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Exp Brain Res (2010) 206:129–139 DOI 10.1007/s00221-010-2198-2 RESEARCH ARTICLE The role of the right temporoparietal junction in intersensory conXict: detection or resolution? Liuba Papeo · Matthew R. Longo · Matteo Feurra · Patrick Haggard Received: 2 December 2009 / Accepted: 13 February 2010 / Published online: 9 March 2010 © Springer-Verlag 2010 Abstract The right temporoparietal junction (rTPJ) is a visual stimulation was incongruent. However, following polysensory cortical area that plays a key role in perception TMS, accuracy improved selectively for D4 in incongruent and awareness. Neuroimaging evidence shows activation of trials, suggesting that the eVects of the conXicting visual rTPJ in intersensory and sensorimotor conXict situations, information were reduced. These Wndings suggest a role but it remains unclear whether this activity reXects detec- of rTPJ in detecting, rather than resolving, intersensory tion or resolution of such conXicts. To address this ques- conXict. tion, we manipulated the relationship between touch and vision using the so-called mirror-box illusion. Participants’ Keywords Visuo-spatial attention · Tactile localization · hands lay on either side of a mirror, which occluded their Finger-speciWcity · Mental body representation · left hand and reXected their right hand, but created the illu- Temporoparietal junction · Intersensory conXict sion that they were looking directly at their left hand. The experimenter simultaneously touched either the middle (D3) or the ring Wnger (D4) of each hand. Participants Introduction judged, which Wnger was touched on their occluded left hand. The visual stimulus corresponding to the touch on the The representation of one’s own body depends on the inte- right hand was therefore either congruent (same Wnger as gration of inputs across several sensory modalities. Signals touch) or incongruent (diVerent Wnger from touch) with the from diVerent modalities are normally consistent and com- task-relevant touch on the left hand. Single-pulse transcra- plementary. In some situations, however, conXicting infor- nial magnetic stimulation (TMS) was delivered to the rTPJ mation is received, and two discrepant sources of immediately after touch. Accuracy in localizing the left information must be integrated (cf. Ernst and BülthoV touch was worse for D4 than for D3, particularly when 2004). Several recent studies have suggested that the tem- poroparietal junction in the right hemisphere (rTPJ) responds to such perceptual conXict. For example, rTPJ was activated by visual information of Wnger movement that was incongruent with proprioception of the actual & L. Papeo ( ) W International School for Advanced Studies, nger movement (Balslev et al. 2005). Likewise, rTPJ SISSA of Trieste, Via Beirut, 2-4, 34014 Trieste, Italy activity increases linearly with increasing temporal delay e-mail: [email protected] between active movement and visual feedback (Leube et al. 2003) and with increasing spatial distortion of visual and M. R. Longo · P. Haggard Institute of Cognitive Neuroscience, proprioceptive information about hand position (Farrer University College London, Alexandra House, et al. 2004). Thus, the rTPJ seems to be associated with 17 Queen Square, London WC1N 3AR, UK intersensory conXict. However, imaging studies have not identiWed the exact role of rTPJ in processing such conXict. M. Feurra Department of Psychology, University of Florence, One hypothesis is that the rTPJ is involved in resolving Via di San Salvi, 12, 50135 Florence, Italy intersensory conXict in order to maintain a coherent percept 123 130 Exp Brain Res (2010) 206:129–139 of the body (Blanke et al. 2004; Blanke and Mohr 2005; Farrer et al. 2004; Spence et al. 1997). When such conXict resolution fails, the normal coherence of the bodily self is replaced by a fragmented or dissociated experience in both clinical (Blanke et al. 2004; Brugger et al. 1997) and healthy populations (Blanke et al. 2005; Farrer et al. 2004; Zacks et al. 1999). Alternatively, rTPJ might simply detect the intersensory discrepancy, with other areas being respon- sible for attempting resolution. This hypothesis Wts with a more general role of the rTPJ in spatial attention to multi- sensory stimuli. Indeed, neuroimaging studies suggest that rTPJ dominates a network of regions responsive to visual, auditory and tactile stimuli and, speciWcally, plays a key role in coding stimuli at an unexpected location or behav- iorally salient changes in external space (AstaWev et al. Fig. 1 2006; Corbetta et al. 1998; Downar et al. 2000; Downar Experimental setup. The participant’s hands lay on either side of a mirror. The participant gazed toward her/his left hand, and there- et al. 2002; see Corbetta and Shulman 2002 for a review). fore saw her/his right hand appearing via the mirror in the left hand’s As such, the rTPJ would be responsible of bottom-up or location. The participant’s Wngers on either hand were touched by stimulus-driven visual attention to detect any relevant means of two sticks, containing a microswitch which triggered TMS 350 ms after the touch onset. TMS was delivered with a coil placed event. This function of the rTPJ is consistent with evidence tangentially over the right TPJ linking lesions in this region to unilateral spatial neglect, a common neuropsychological syndrome following injury to the right hemisphere, in which salient stimuli in the left touch, is improved when visual and tactile stimulations are hemispace fail to attract attention and reach awareness at congruent locations and is disrupted when the two loca- (Bisiach et al. 1996; Friedrich et al. 1998; Mort et al. 2003; tions are incongruent (Spence et al. 1998; Pavani et al. Vallar 2001). 2000). The inXuence of vision on tactile discrimination is We created conXict between vision and touch using a also suggested by eVects of seeing the body on somatosen- tactile version of the mirror-box illusion, previously used to sation, whereby even non-informative view of body parts investigate phantom limbs (Ramachandran and Rogers- increases tactile acuity (e.g., Haggard 2006; Kennett et al. Ramachandran 1996; Ramachandran et al. 1995), percep- 2001) and suppresses acute pain (Longo et al. 2009). On tual conXict (e.g., Fink et al. 1999; Holmes et al. 2006) and this basis, the bodily visual information was expected to eVects of vision on somatosensory processing (e.g., Harris create a transfer of tactile sensation from one Wnger to et al. 2007; Longo et al. 2009). Participants placed their another in the incongruent condition, even if participants hands on either side of a mirror aligned with their sagittal were aware of the potential conXict. Indeed, Ro et al. plane, in the setup shown in Fig. 1. Looking into the mirror, (2004) reported anecdotally that the illusion of seeing one’s the reXection of their right hand appeared to be a direct hand touched in the mirror box could generate tactile sensa- view of their left hand. The experimenter synchronously tions on a non-stimulated hand. touched either the middle (D3) or the ring Wnger (D4) of In one condition, we delivered single-pulse transcranial both hands. Participants judged which Wnger on their magnetic stimulation (TMS) to the rTPJ to alter its activity occluded left hand was touched. Touch could either be con- and thus investigate its role in intersensory conXict. We gruent or incongruent with vision. When touch was congru- stimulated the right side only, because the right—but not ent with vision, the same Wnger was touched on left and the left—TPJ is held to process multisensory body-related right hand. What participants saw was therefore congruent information (Blanke and Mohr 2005) and portions of this with what they felt on their target left hand. When touch region have been related to the awareness of personal space was incongruent, D3 was touched on the right hand and D4 (Committeri et al. 2007). Generally, clinical (Vallar 1998), on the left, or vice versa. Therefore, what participants saw TMS (Chambers et al. 2004) and functional neuroimaging was incongruent with what they felt. studies (Nobre et al. 2007) indicate a right hemispheric Several phenomena hold that vision dominates over dominance for visuo-spatial attention, which was crucial touch. For instance, in crossmodal congruence task, partici- for our task. In fact, given their perceptual similarity, pants receive tactile stimulation on one Wnger, while a non- Wngers are mostly identiWed by their position through bodily visual distractor (e.g., a circle) appears proximal to visuo-spatial exploration (Goldenberg 1999). Accordingly, the hand position. Tactile discrimination, the ability to their perceptual discrimination is particularly vulnerable to diVerentiate information received through the sense of interference and narrowing of visual attention. Indeed, 123 Exp Brain Res (2010) 206:129–139 131 patients with damage to the right hemisphere may show of each hand, with two identical wooden sticks. A micro- selective impairment in processing Wnger postures (Golden- switch attached to the stick touching the left hand triggered berg 1999) as part of generally impaired perceptual analy- TMS and the audio recording. The touches were punctuate sis. Recently, a strong association has been reported and clearly suprathreshold. We instructed participants to between the severity of left-sided spatial neglect and dis- look into the mirror and verbally report, which Wnger was turbed imitation of Wnger posture, as it poses high demand touched on their left hand