Spatial orienting by left hemisphere language areas: a relict from the past?

doi:10.1093/brain/awr120 Brain 2011: 134; 3059–3070 | 3059 BRAIN A JOURNAL OF NEUROLOGY Spatial orienting by left hemisphere language areas: a relict from the past? Julia Suchan1 and Hans-Otto Karnath1,2 1 Centre of Neurology, Division of Neuropsychology, Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany 2 Centre for Advanced Brain Imaging, Georgia Institute of Technology, Atlanta GA, USA Correspondence to: Prof. Hans-Otto Karnath, MD PhD, Centre of Neurology, University of Tübingen, Hoppe-Seyler-Str.3, D-72076 Tübingen, Germany E-mail: During evolution, the human brain developed remarkable functional differences between left and right hemispheres. Due to this lateralization, disorders of spatial orienting occur predominantly after right brain damage and disorders of language after left brain damage. In contrast to this general pattern, few individuals show disturbed spatial orienting (spatial neglect) after left brain damage. Using a voxel-based lesion analysis approach, we found that neglect after acute left brain damage is represented in areas typically serving language functions, namely the superior and middle temporal gyri, inferior parietal lobule and insula. Since all except one of these patients also suffered from aphasia, we conclude that lateralization is not just reversed but that both functions (language and spatial orienting) rather are represented in the same left hemisphere regions. We speculate that a representation of spatial orienting in left hemisphere language areas might be a phylogenetic relict in humans, though this representation stays subdominant in the vast majority of individuals. Keywords: hemispheric specialization; spatial neglect; aphasia; lateralization; left brain damage Introduction During evolution, the human brain has developed fascinating functional differences between the left and right hemisphere. Language is the oldest and the best-known example for such a lateralization. The first historical findings about left cerebral dominance for language come from post-mortem examinations in neurological patients (e.g. Broca, 1861; Dax, 1865). The nature of the mechanisms underlying these cerebral asymmetries still remains unclear (Badzakova-Trajkov et al., 2010). Genetic models claim that the RS gene, for example, might be responsible for the asymmetry of the language system. If this gene is present, it supports lateralization for a dominant left hemisphere for language; if the opposite is true, lateralization occurs by chance (Alexander and Annett, 1996). Several authors have suggested that the left lateralization of language causes other functions such as spatial orienting to be lateralized in the right hemisphere (e.g. Corballis and Morgan, 1978; Corballis, 1981; Cook, 1984). Hellige (1990) assumed that at birth the right hemisphere is more mature than the left. The right hemisphere thus is more influenced from incoming visual information and is specialized for attentional processes rather than for language. Previc (1991) hypothesized that there is a developmental right ear advantage at birth that leads to language dominance in the left hemisphere, whereas a developmental otholith advantage on the left side causes dominant representation of visuospatial functions in the right hemisphere. The hemispheric lateralization of cognitive functions is evident in brain injury. Disorders of language (aphasia) occur predominantly after left brain damage and disorders of spatial orienting and Received January 7, 2011. Revised April 8, 2011. Accepted April 11, 2011. Advance Access publication May 30, 2011 ß The Author (2011). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: 3060 | Brain 2011: 134; 3059–3070 attention (spatial neglect) predominantly after right brain damage (Dax, 1865; Marsh et al., 2006; Becker and Karnath, 2007). Also, functional MRI studies in healthy subjects have revealed a clear lateralization of language in the left and spatial orienting and attention in the right hemisphere. However, these studies have also demonstrated—though less prominently—involvement of homologous areas in the respective ‘non-dominant’ hemisphere, i.e. the right for language and the left for spatial orienting (e.g. Himmelbach et al., 2006; Vigneau et al., 2006; Tzourio-Mazoyer et al., 2010). The role of this activity in the respective non-dominant hemisphere is still unclear. Thus investigation of individuals who—in contrast to the general pattern—show disturbance of lateralized cognitive functions after a lesion in the non-dominant hemisphere is interesting. The present study concentrates on disturbed spatial orienting and attention following left brain damage. While the vast majority of patients with spatial neglect suffer from right hemisphere damage, some individuals show spatial neglect after left brain damage (Becker and Karnath, 2007). These subjects demonstrate a bias in perception and action towards the ipsilesional left side of space and typically fail to address stimuli located on the right. The existence of such patients demonstrates that the group of subjects with disturbed spatial orientation is not a homogenous group (as is the case for the observation of patients with aphasia following right brain damage). These ‘exceptions from the rule’ provide an opportunity to gain deeper insights into the representation of spatial orienting in the human brain. Despite its impact for our understanding of hemispheric lateralization of cognitive functions, little is known about neglect after left brain damage (Beis et al., 2004; Kleinman et al., 2007). It was reported to be less severe than neglect after right brain damage (Ogden, 1987) or that patients with neglect with left brain damage show a different pattern in cancellation tasks compared with patients with right brain damage with neglect (Gainotti et al., 1990; Halligan et al., 1992). Symptoms typically associated with spatial neglect after left brain damage are aphasia, apraxia and/or disturbed prosody (e.g. Selnes et al., 1982, 1991; Kellar and Levick, 1985; Fischer et al., 1991). Also, little is known about the brain areas within the left hemisphere that cause spatial neglect when lesioned. Most studies reported single cases or small groups. Lesions of these patients were described to be large, covering frontal, temporal and parietal regions (Selnes et al., 1982, 1991; Kellar and Levick, 1985; Junqué et al., 1986; Cohen et al., 1991; Fischer et al., 1991; Posteraro and Maravita, 1996; Kleinman et al., 2007). Only few studies investigated larger samples of patients with left brain damage with spatial neglect. Ogden (1985) compared 28 patients with left brain damage and 20 patients with right brain damage with neglect and suggested that neglect patients with left brain damage have more anterior located lesions than neglect patients with right brain damage. Mae (...truncated)