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doi:10.

1093/brain/awn089

Brain (2008), 131, 1414 ^1415

SCIENTIF IC COMMENTARY

The anatomy of blindsight
Part of every neurological examination is an assessment of the visual field, obtained by asking patients to detect the presence of test targets on a defined background. Clinicians use either visual field testing to confrontation or more careful mapping and quantification of sensitivity of the visual field using automated perimetry. All of these approaches rely on the patient indicating whether they are aware of the presence of a test target at a particular location. Such testing can establish the presence of scotomas or blind regions of the visual field, where patients report that they do not perceive anything presented in such regions. Systematic correspondences between the location of visual field defects and the site of brain damage in the occipital lobe are sufficient to permit determination of a retinotopic map or projection of the retinal image onto what is now known as primary visual cortex (V1) on the medial surface of the occipital lobe (Inouye, 1909). Damage to V1 is thus associated with a lack of awareness for stimuli presented at corresponding points in the visual field, consistent with a role for V1 in visual awareness (Rees, 2007). However, during visual field testing, few if any clinicians would routinely press their patients to try and guess properties of stimuli that they resolutely deny being able to see when they are presented in a scotoma. But, when such a systematic investigation is performed using forced-choice procedures, remarkably, some patients show residual visual capacity in their blind field. These patients are able to perform certain discriminations and localizations better than chance in the acknowledged absence of awareness. This ability has become known as ‘blindsight’. We review the classic first report in detail (Weiskrantz et al., 1974) of such an individual, D.B., in From the Archives (page 1411). Subsequently, a number of other individuals with blindsight have been described and subject to intensive investigation (see Stoerig and Cowey, 2007 or Zeki and Ffytche, 1998 for reviews). While a number of functional magnetic resonance imaging studies have been carried out that describe the brain activity underpinning such discriminations without awareness, the structural basis for the preserved visual abilities has, until now, remained particularly unclear. In the current issue of Brain, Bridge and colleagues present new evidence for anatomical connections underlying such blindsight abilities (page 1433). They present diffusion tensor MRI measurements that compare a wellstudied individual with blindsight to control subjects. Blindsight subject G.Y. is a 53-year-old individual who has a large left medial occipital lesion and a rather smaller right parietal lesion, caused by a traffic accident at the age of 8 (Barbur et al., 1980). Striate cortex is absent in his left hemisphere except at the occipital pole and he has a corresponding right hemianopia with some three to four degrees of macular sparing. Bridge and colleagues obtained diffusion weighted MR images that provide information about the diffusion of water at each voxel in the MR image in the form of diffusion tensors. These diffusion tensors were visualized using probabilistic tractography, which identifies white matter tracts oriented along the direction of maximal water diffusion of the voxels they pass through, while also providing information about the directional uncertainty and strength of the tracts that are generated. This allows determination of a connectivity index and provides a metric for assessing the reliability and strength of the white matter pathways generated. There are three principal findings from these investigations, which focus on anatomical structures in the early visual pathway. Both G.Y. and normal controls show a tract connecting the lateral geniculate nucleus (LGN) to the ipsilateral visual motion area V5/MT that bypasses V1. But G.Y. also displays two strong differences with controls. First, crossing white matter tracts are present that connect the LGN with contralateral V5/MT. These tracts run through the splenium and are absent or vestigial in healthy control subjects without occipital damage. Second, G.Y. shows a very substantial trancallosal connection between V5/MT bilaterally. One of the strengths of this study is the combination of state-of-the-art probabilistic tractography with careful attention to control analyses. Tractography can be problematic when carried out in proximity to regions of low anisotropy like G.Y.’ s lesion. Thus, one important concern is whether the presence of a large left occipital lesion might increase the likelihood of the tractography algorithm tracing a path from LGN through the corpus callosum, thus giving the artefactual appearance of crossing tracts in G.Y. However, three additional control analyses in which the starting location for the tractography algorithm was varied between LGN, the splenium and V5/MT did not affect the findings, suggesting that the presence of crossed pathways between LGN and V5/MT in G.Y. is not an artefact induced by his lesion. Similarly, the age of subjects can also influence tractography results through atrophy and partial volume effects. Therefore, it is reassuring that the comparisons of G.Y. and control subjects are identical whether the control subjects are young or age-matched. How do these novel anatomical findings advance our knowledge of the mechanisms of blindsight? The crossed

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Scientific Commentary pathways between LGN and V5/MT demonstrated in the present study can account nicely for some previously published data, such as the presence of ipsilateral (as well as contralateral) V5/MT activation to stimuli presented in his (sighted) left hemifield (e.g. Morland et al., 2004). And increased interhemispheric connectivity is consistent with the observation that transcranial magnetic stimulation can elicit phosphenes when applied to V5/MT bilaterally in G.Y. but not when applied to left V5/MT alone (Silvanto et al., 2007), suggesting a requirement for interhemispheric connectivity. But although crossed pathways might suggest right V5/MT activation in response to stimulation of his (blind) right visual field as a potential mechanism underlying his ability to perform visual discriminations in the absence of awareness, only one study has shown such activation (Goebel et al., 2001). Others implicate contralateral (left) V5/MT (Barbur et al., 1993) or lateral occipital regions (Morland et al., 2004). Thus, while these anatomical tracts demonstrated in G.Y. are broadly consistent with the notion of V5/MT and interhemispheric information transmission mediating blindsight abilities, a more detailed account will require considerably more work to reconcile these apparently conflicting issues. One possible approach will be to combine this new anatomical information with approaches such as Dynamic Causal Modelling (Friston et al., 2003) that can establish differences in coupling between brain areas, using data obtained from noninvasive measurements such as functional MRI or magnetoencephalography. How did such crossed LGN-V5/MT and interhemispheric tracts arise in G.Y.? G.Y. suffered brain injury at the age of 8, but some cortico-cortical connections (for example, those indirectly indexed by the cross-sectional area of the corpus callosum) continue to grow until adulthood. Thus, some of the plasticity observed in G.Y.’ s brain may have emerged through strengthening of existing connections during brain growth and maturation in late childhood and adolescence. But the crossed pathways between LGN and V5/MT are pathways not present in normal controls, so may represent new connections. There is a precedent for this in the literature, as patients who have undergone hemispherectomy and exhibit blindsight have projections from the superior colliculus to the contralateral hemisphere that are not seen in similar patients without blindsight (Leh et al., 2006). The possibility of such large-scale plasticity is intriguing and merits further inquiry. Finally, it remains a logical possibility that the tracts identified in G.Y. existed prior to his injury, and thus account for his ability to show blindsight that emerged following brain injury. More generally, the notion that patients like G.Y. are highly unusual and that most patients with damage to V1

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do not exhibit blindsight remains under active debate. As mentioned previously, blindsight can only be uncovered using forced-choice methods and so conventional clinical approaches do not test for blindsight, as patients typically claim they see nothing in their field defect with perimetry. This conventional approach to clinical practice may, therefore, underestimate the prevalence of blindsight. Indeed, when systematic forced-choice testing with stimuli matched appropriately to the spatial and temporal characteristics of the residual vision found in blindsight, has been applied to patients with visual field defects resulting from occipital damage, the majority demonstrate blindsight (Sahraie et al., 2006).

Geraint Rees Institute of Cognitive Neuroscience & Wellcome Trust Centre for Neuroimaging, University College London, 17 Queen Square, London WC1N 3AR, UK E-mail: g.rees@fil.ion.ucl.ac.uk

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