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      Temporoparietal encoding of space and time during vestibular-guided orientation

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          Abstract

          The cardinal features of vestibular dysfunction are illusory self-motion (vertigo) and spatial disorientation. Testing 18 acute focal cortical lesion patients, Kaski et al. show that temporoparietal junction lesions impair vestibular-guided spatial orientation but not self-motion perception. Distinct cortical substrates thus mediate the vestibular percepts of spatial orientation and self-motion.

          Abstract

          The cardinal features of vestibular dysfunction are illusory self-motion (vertigo) and spatial disorientation. Testing 18 acute focal cortical lesion patients, Kaski et al. show that temporoparietal junction lesions impair vestibular-guided spatial orientation but not self-motion perception. Distinct cortical substrates thus mediate the vestibular percepts of spatial orientation and self-motion.

          Abstract

          When we walk in our environment, we readily determine our travelled distance and location using visual cues. In the dark, estimating travelled distance uses a combination of somatosensory and vestibular (i.e. inertial) cues. The observed inability of patients with complete peripheral vestibular failure to update their angular travelled distance during active or passive turns in the dark implies a privileged role for vestibular cues during human angular orientation. As vestibular signals only provide inertial cues of self-motion (e.g. velocity, °/s), the brain must convert motion information to distance information (a process called ‘path integration’) to maintain our spatial orientation during self-motion in the dark. It is unknown, however, what brain areas are involved in converting vestibular-motion signals to those that enable such vestibular-spatial orientation. Hence, using voxel-based lesion–symptom mapping techniques, we explored the effect of acute right hemisphere lesions in 18 patients on perceived angular position, velocity and motion duration during whole-body angular rotations in the dark. First, compared to healthy controls’ spatial orientation performance, we found that of the 18 acute stroke patients tested, only the four patients with damage to the temporoparietal junction showed impaired spatial orientation performance for leftward (contralesional) compared to rightward (ipsilesional) rotations. Second, only patients with temporoparietal junction damage showed a congruent underestimation in both their travelled distance (perceived as shorter) and motion duration (perceived as briefer) for leftward compared to rightward rotations. All 18 lesion patients tested showed normal self-motion perception. These data suggest that the cerebral cortical regions mediating vestibular-motion (‘am I moving?’) and vestibular-spatial perception (‘where am I?’) are distinct. Furthermore, the congruent contralesional deficit in time (motion duration) and position perception, seen only in temporoparietal junction patients, may reflect a common neural substrate in the temporoparietal junction that mediates the encoding of motion duration and travelled distance during vestibular-guided navigation. Alternatively, the deficits in timing and spatial orientation with temporoparietal junction lesions could be functionally linked, implying that the temporoparietal junction may act as a cortical temporal integrator, combining estimates of self-motion velocity over time to derive an estimate of travelled distance. This intriguing possibility predicts that timing abnormalities could lead to spatial disorientation.

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          Most cited references43

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          A clinical sign of canal paresis.

          Unilateral loss of horizontal semicircular canal function, termed canal paresis, is an important finding in dizzy patients. To our knowledge, apart from head-shaking nystagmus, no clinical sign of canal paresis has yet been described and the term derives from the characteristic finding on caloric tests: little or no nystagmus evoked by either hot or cold irrigation of the affected ear. We describe a simple and reliable clinical sign of total unilateral loss of horizontal semicircular canal function: one large or several small oppositely directed, compensatory, refixation saccades elicited by rapid horizontal head rotation toward the lesioned side. Using magnetic search coils to measure head and eye movement, we have validated this sign in 12 patients who had undergone unilateral vestibular neurectomy.
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            Using human brain lesions to infer function: a relic from a past era in the fMRI age?

            Recent technological advances, such as functional imaging techniques, allow neuroscientists to measure and localize brain activity in healthy individuals. These techniques avoid many of the limitations of the traditional method for inferring brain function, which relies on examining patients with brain lesions. This has fueled the zeitgeist that the classical lesion method is an inferior and perhaps obsolescent technique. However, although the lesion method has important weaknesses, we argue that it complements the newer activation methods (and their weaknesses). Furthermore, recent developments can address many of the criticisms of the lesion method. Patients with brain lesions provide a unique window into brain function, and this approach will fill an important niche in future research.
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              The anatomy of visual neglect.

              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 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 findings challenge the recent influential proposal that lesions of this area are critically associated with neglect. Instead, our results implicate the angular gyrus and parahippocampal region in this role.
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                Author and article information

                Journal
                Brain
                Brain
                brainj
                brain
                Brain
                Oxford University Press
                0006-8950
                1460-2156
                February 2016
                30 December 2015
                30 December 2015
                : 139
                : 2
                : 392-403
                Affiliations
                Division of Brain Sciences, Imperial College London, London W6 8RF, UK
                Author notes
                Correspondence to: Barry M Seemungal, Division of Brain Sciences, Imperial College London, Charing Cross Campus, London W6 8RF, UK E-mail: b.seemungal@ 123456imperial.ac.uk or barseem@ 123456gmail.com
                Article
                awv370
                10.1093/brain/awv370
                4805090
                26719385
                a212f918-79f1-4573-9750-9d83d05302e1
                © The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 30 April 2015
                : 15 October 2015
                : 26 October 2015
                Page count
                Pages: 12
                Categories
                Original Articles

                Neurosciences
                vestibular perception,spatial orientation,time perception,path-integration,temporo-parietal junction

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