The anatomy of visual neglect

DOI: 10.1093/brain/awg200 Advanced Access publication June 23, 2003 Brain (2003), 126, 1986±1997 The anatomy of visual neglect Dominic J. Mort,1 Paresh Malhotra,1,2 Sabira K. Mannan,1 Chris Rorden,3 Alidz Pambakian,1 Chris Kennard1 and Masud Husain1,2 1Division of Neuroscience and Psychological Medicine, Imperial College, 2Institute of Cognitive Neuroscience, University College London, Queen Square, London and 3Department of Psychology, University of Nottingham, Nottingham, UK Summary The brain regions that are critically associated with visual neglect have become intensely disputed. In particular, one study of middle cerebral artery (MCA) stroke patients has claimed that the key brain region associated with neglect is the mid portion of the superior temporal gyrus (STG), on the lateral surface of the right hemisphere, rather than the posterior parietal lobe. Such a result has wide-ranging implications for both our understanding of the normal function these cortical areas and the potential mechanisms underlying neglect. Here, we use novel high resolution MRI protocols to map the lesions of 35 right-hemisphere patients who had suffered either MCA or posterior cerebral artery (PCA) territory stroke. For patients with MCA territory strokes, the critical area involved in all neglect Correspondence to: Masud Husain, Division of Neuroscience and Psychological Medicine, Imperial College, Charing Cross Hospital Campus, London W6 8RF, UK E-mail: patients was the angular gyrus of the inferior parietal lobe (IPL). Although the STG was damaged in half of our MCA neglect patients, it was spared in the rest. For PCA territory strokes, all patients with neglect had lesions involving the parahippocampal region, on the medial surface of the temporal lobe. PCA patients without neglect did not have damage to this area. We conclude that damage to two posterior regions, one in the IPL and the other in the medial temporal lobe, is associated with neglect. Although some neglect patients do have damage to the STG, our ®ndings challenge the recent in¯uential proposal that lesions of this area are critically associated with neglect. Instead, our results implicate the angular gyrus and parahippocampal region in this role. Keywords: neglect; parietal; temporal; angular gyrus; parahippocampal region Abbreviations: ANG = angular gyrus; IFG = inferior frontal gyrus; IPL = inferior parietal lobe; IPS = intraparietal sulcus; LF = lateral ®ssure; MCA = middle cerebral artery; MFG = middle frontal gyrus; MNI = Montreal Neurological Institute; PCA = posterior cerebral artery; ROI = region of interest; SMG = supramarginal gyrus; SPL = superior parietal lobe; STG = superior temporal gyrus; STS = superior temporal sulcus; TPJ = temporoparietal junction Introduction The search for those brain areas that, when damaged, are capable of producing visual neglect has become the subject of intense debate (Karnath and Himmelbach, 2002; Marshall et al., 2002). Until recently, in case series of unselected middle cerebral artery (MCA) patients who typically have large strokes, the most consistent observation has been that the brain area most commonly associated with neglect is the right posterior parietal lobe, particularly the region around the temporoparietal junction (TPJ) (Heilman et al., 1983; Vallar and Perani, 1986; Leibovitch et al., 1998; Vallar, 2001). Neglect has also been observed following more focal strokes of the right inferior frontal lobe (Husain and Kennard, 1996) and subcortical structures such as the thalamus (Cambier et al., 1980) and basal ganglia (Damasio et al., 1980; Karnath et al., 2002), although accompanying hypoperfusion of Brain 126 ã Guarantors of Brain 2003; all rights reserved overlying cortex may be an important determinant of neglect in subcortical cases (Vallar et al., 1988; Hillis et al., 2002). In addition to these locationsÐall within the territory perfused by the MCAÐthere have been reports of neglect following strokes in the territory of the posterior cerebral artery (PCA), but the exact medial occipito-temporal regions critical for neglect have not been de®ned (Doricchi and Angelelli, 1999; Cals et al., 2002). Vallar and Perani (1986) noted that the syndrome was usually absent when infarction was limited to the occipital lobe, as has a more recent study which reported that neglect occurred in nine out of 53 patients with isolated super®cial right PCA strokes (Cals et al., 2002). This study also observed that neglect was more frequent in patients with occipital infarcts that extended more anteriorly, although lesions were not plotted. In another study, lesion Anatomy of visual neglect reconstructions demonstrated medial temporal lobe involvement, but the plots also included posterior MCA territory strokes (Doricchi and Angelelli, 1999). Moreover, there was no lesion contrast made with PCA controls without neglect, so it is not possible to distinguish between the PCA territory regions speci®cally involved with neglect and those regions that are typically damaged following PCA lesions. Almost all previous anatomical series of neglect have used CT imaging (but see Maguire and Ogden, 2002). Although the best in-plane resolution of most CT scans is very good (0.3±0.5 mm), the slice thickness (or z-plane resolution) is much larger, typically 8±10 mm. This is one important limiting factor for lesion reconstruction using this imaging modality. Thus, in the published literature, reconstructions from CT are relatively coarse, typically showing 10 or often fewer slices (e.g. Husain et al., 1997). Moreover, if scans are acquired for clinical purposes and do not follow a strict research protocol (as used, for example, by Friedrich et al., 1998), the orientation of these slices will vary slightly across patients. Thus they may not match exactly the templates onto which the lesions will be placed, even if several different templates are used. Finally, standard practice is to draw the lesions by hand onto templates. Although some investigators develop great expertise in this, lesion reconstruction in this manner is observer dependent. All these factors limit the spatial accuracy of standard CT-acquired reconstructions. A recent study of MCA patients, in which MRI was available for many of the participants, came to a radically different conclusion from previous investigations, implicating a region along the right mid superior temporal gyrus (STG) as the critical zone associated with neglect (Karnath et al., 2001). Note that this region of the STG is not the posterior portion that has sometimes been taken to be part of the TPJ. If this new result is correct, it would have potentially far-reaching consequences for our understanding of the mechanisms underlying neglect, as well as of the normal functions of both the posterior parietal lobe (the region previously implicated in neglect) and the STG in healthy individuals (Karnath, 2001). However, the study had several important drawb (...truncated)