Neural bases of personal and extrapersonal neglect in humans

Abstract

Human awareness of left space may be disrupted by cerebral lesions to the right hemisphere (hemispatial neglect). Current knowledge on the anatomical bases of this complex syndrome is based on the results of group studies that investigated primarily the best known aspect of the syndrome, which is visual neglect for near extrapersonal (or peripersonal) space. However, another component-neglect for personal space-is more often associated with, than double-dissociated from, extrapersonal neglect, especially, in chronic patients. The present investigation aimed at exploring the anatomical substrate of both extrapersonal and personal neglect by using different advanced methodological approaches to lesion-function correlation. Fifty-two right ischaemic patients were submitted to neuropsychological assessment and in-depth MRI evaluation. The borders of each patient's lesion were delimited onto its own high-resolution anatomical image and then submitted to an automated spatial normalization algorithm. Besides conventional lesion density plots and subtraction analysis, region-based statistical analyses were performed on percentage values of the lesioned tissue also using a new parcellation of the white matter (WM). Data were finally submitted to voxelwise statistical analysis using a recently proposed method (voxel-based lesion-symptom mapping). Results converged in showing that awareness of extrapersonal space is based on the integrity of a circuit of right frontal (ventral premotor cortex and middle frontal gyrus) and superior temporal regions, whereas awareness of personal space is rooted in right inferior parietal regions (supramarginal gyrus, post-central gyrus and especially the WM medial to them). Common but less crucial regions for both neglect sub-types were located in the temporo-peri-Sylvian cortex. We suggest that extrapersonal space awareness critically involves a ventral circuit recently described for the exogenous allocation and reorienting of attention in space. Disruption of personal space awareness, instead, seems to be due to a functional disconnection between regions important for coding proprioceptive and somatosensory inputs, and regions coding more abstract egocentric representations of the body in space. In conclusion, present data strongly support a segregation of personal and extrapersonal spatial awareness in humans, both from a functional and an anatomical point of view.

Bodily ownership and self-location: Components of bodily self-consciousness

“…Patients with PPc lesions are strongly impaired when performing tasks requiring on-line coding of body posture (Schwoebel & Coslett, 2005), when attending to body parts on the left in the case of a right lesion (i.e. personal neglect; Committeri et al, 2007) and when describing the spatial relations between body parts in the case of a left lesion (i.e. autotopagnosia; Ogden, 1985).…”

Differential Involvement of Somatosensory and Interoceptive Cortices during the Observation of Affective Touch

“…Neuropsychological and neurophysiological studies suggest that RH TPJ contributes to multisensory integration of bodily information underlying a conscious and coherent experience of the bodily self (e.g., Committeri et al, 2007;Blanke et al, 2005;Berlucchi & Aglioti, 1997). Transcranial magnetic stimulation studies investigating the RHI showed that disruption of RH TPJ reduced the extent to which an observed prosthetic rubber hand stroked in synchrony with oneʼs own, unseen, hand was incorporated into the mental representation of oneʼs own body as measured by proprioceptive drift, whereas it did not affect subjective feelings of ownership, the latter likely mediated by pIC (Kammers et al, 2009;Tsakiris, Costantini, & Haggard, 2008).…”

The role of the right temporoparietal junction in intersensory conflict: detection or resolution?

“…We stimulated the right side only, because the right -but not the left -TPJ is held to process multisensory body-related information and portions of this region have been related to the awareness of personal space (Committeri et al 2007). Generally, clinical (Vallar 1998), TMS (Chambers et al 2004) and functional neuroimaging studies (Nobre et al 1997) indicate a right hemispheric dominance for visuo-spatial attention, which was crucial for our task.…”