Decoding the anatomical network of spatial attention.
ABSTRACT: The study of stroke patients with modern lesion-symptom analysis techniques has yielded valuable insights into the representation of spatial attention in the human brain. Here we introduce an approach--multivariate pattern analysis--that no longer assumes independent contributions of brain regions but rather quantifies the joint contribution of multiple brain regions in determining behavior. In a large sample of stroke patients, we found patterns of damage more predictive of spatial neglect than the best-performing single voxel. In addition, modeling multiple brain regions--those that are frequently damaged and, importantly, spared--provided more predictive information than modeling single regions. Interestingly, we also found that the superior temporal gyrus demonstrated a consistent ability to improve classifier performance when added to other regions, implying uniquely predictive information. In sharp contrast, classifier performance for both the angular gyrus and insular cortex was reliably enhanced by the addition of other brain regions, suggesting these regions lack independent predictive information for spatial neglect. Our findings highlight the utility of multivariate pattern analysis in lesion mapping, furnishing neuroscience with a modern approach for using lesion data to study human brain function.
Project description:Spatial neglect is a characterized by a failure to attend or make movements towards left-sided stimuli. Common paper-and-pencil tasks to diagnose spatial neglect are sensitive to perseverative errors, including additional marks over already cancelled targets and "scribbling" out a target. Here, we examine whether functionally distinct perseverative behaviors are related to spatial neglect. Line cancellation tasks of 45 healthy controls and 220 right-hemisphere stroke survivors were examined for recurrent marks (RM) and continuous marks (CM) perseverations. We found that RM perseveration correlated with neglect severity, while CM perseveration did not. Examination of lesion profiles for the two groups indicated distinct anatomical correlates, with RM lesions overlapping regions implicated in spatial neglect including the rolandic operculum, superior temporal gyrus, and inferior parietal lobule.
Project description:We contrasted the neuroanatomical substrates of sub-acute and chronic visuospatial deficits associated with different aspects of unilateral neglect using computed tomography scans acquired as part of routine clinical diagnosis. Voxel-wise statistical analyses were conducted on a group of 160 stroke patients scanned at a sub-acute stage. Lesion-deficit relationships were assessed across the whole brain, separately for grey and white matter. We assessed lesions that were associated with behavioural performance (i) at a sub-acute stage (within 3 months of the stroke) and (ii) at a chronic stage (after 9 months post stroke). Allocentric and egocentric neglect symptoms at the sub-acute stage were associated with lesions to dissociated regions within the frontal lobe, amongst other regions. However the frontal lesions were not associated with neglect at the chronic stage. On the other hand, lesions in the angular gyrus were associated with persistent allocentric neglect. In contrast, lesions within the superior temporal gyrus extending into the supramarginal gyrus, as well as lesions within the basal ganglia and insula, were associated with persistent egocentric neglect. Damage within the temporo-parietal junction was associated with both types of neglect at the sub-acute stage and 9 months later. Furthermore, white matter disconnections resulting from damage along the superior longitudinal fasciculus were associated with both types of neglect and critically related to both sub-acute and chronic deficits. Finally, there was a significant difference in the lesion volume between patients who recovered from neglect and patients with chronic deficits. The findings presented provide evidence that (i) the lesion location and lesion size can be used to successfully predict the outcome of neglect based on clinical CT scans, (ii) lesion location alone can serve as a critical predictor for persistent neglect symptoms, (iii) wide spread lesions are associated with neglect symptoms at the sub-acute stage but only some of these are critical for predicting whether neglect will become a chronic disorder and (iv) the severity of behavioural symptoms can be a useful predictor of recovery in the absence of neuroimaging findings on clinical scans. We discuss the implications for understanding the symptoms of the neglect syndrome, the recovery of function and the use of clinical scans to predict outcome.
Project description:UNLABELLED:Although acquired amusia is a relatively common disorder after stroke, its precise neuroanatomical basis is still unknown. To evaluate which brain regions form the neural substrate for acquired amusia and its recovery, we performed a voxel-based lesion-symptom mapping (VLSM) and morphometry (VBM) study with 77 human stroke subjects. Structural MRIs were acquired at acute and 6 month poststroke stages. Amusia and aphasia were behaviorally assessed at acute and 3 month poststroke stages using the Scale and Rhythm subtests of the Montreal Battery of Evaluation of Amusia (MBEA) and language tests. VLSM analyses indicated that amusia was associated with a lesion area comprising the superior temporal gyrus, Heschl's gyrus, insula, and striatum in the right hemisphere, clearly different from the lesion pattern associated with aphasia. Parametric analyses of MBEA Pitch and Rhythm scores showed extensive lesion overlap in the right striatum, as well as in the right Heschl's gyrus and superior temporal gyrus. Lesions associated with Rhythm scores extended more superiorly and posterolaterally. VBM analysis of volume changes from the acute to the 6 month stage showed a clear decrease in gray matter volume in the right superior and middle temporal gyri in nonrecovered amusic patients compared with nonamusic patients. This increased atrophy was more evident in anterior temporal areas in rhythm amusia and in posterior temporal and temporoparietal areas in pitch amusia. Overall, the results implicate right temporal and subcortical regions as the crucial neural substrate for acquired amusia and highlight the importance of different temporal lobe regions for the recovery of amusia after stroke. SIGNIFICANCE STATEMENT:Lesion studies are essential in uncovering the brain regions causally linked to a given behavior or skill. For music perception ability, previous lesion studies of amusia have been methodologically limited in both spatial accuracy and time domain as well as by small sample sizes, providing coarse and equivocal information about which brain areas underlie amusia. By using longitudinal MRI and behavioral data from a large sample of stroke patients coupled with modern voxel-based analyses methods, we were able provide the first systematic evidence for the causal role of right temporal and striatal areas in music perception. Clinically, these results have important implications for the diagnosis and prognosis of amusia after stroke and for rehabilitation planning.
Project description:Visual neglect results from dysfunction within the spatial attention network. The structural connectivity in undamaged brain tissue in neglect has barely been investigated until now. In the present study, we explored the microstructural white matter characteristics of the contralesional hemisphere in relation to neglect severity and recovery in acute stroke patients. We compared age-matched healthy subjects and three groups of acute stroke patients (9?±?0.5 days after stroke): (i) patients with nonrecovered neglect (n?=?12); (ii) patients with rapid recovery from initial neglect (within the first week post-stroke, n?=?7), (iii) stroke patients without neglect (n?=?17). We analyzed the differences between groups in grey and white matter density and fractional anisotropy (FA) and used fiber tracking to identify the affected fibers. Patients with nonrecovered neglect differed from those with rapid recovery by FA-reduction in the left inferior parietal lobe. Fibers passing through this region connect the left-hemispheric analogues of the ventral attention system. Compared with healthy subjects, neglect patients with persisting neglect had FA-reduction in the left superior parietal lobe, optic radiation, and left corpus callosum/cingulum. Fibers passing through these regions connect centers of the left dorsal attention system. FA-reduction in the identified regions correlated with neglect severity. The study shows for the first time white matter changes within the spatial attention system remote from the lesion and correlating with the extent and persistence of neglect. The data support the concept of neglect as disintegration within the whole attention system and illustrate the dynamics of structural-functional correlates in acute stroke.
Project description:The pursuit of relating the location of neural damage to the pattern of acquired language and general cognitive deficits post-stroke stems back to the 19th century behavioural neurology. While spatial specificity has improved dramatically over time, from the large areas of damage specified by post-mortem investigation to the millimetre precision of modern MRI, there is an underlying issue that is rarely addressed, which relates to the fact that damage to a given area of the brain is not random but constrained by the brain's vasculature. Accordingly, the aim of this study was to uncover the statistical structure underlying the lesion profile in chronic aphasia post-stroke. By applying varimax-rotated principal component analysis to the lesions of 70 patients with chronic post-stroke aphasia, we identified 17 interpretable clusters, largely reflecting the vascular supply of middle cerebral artery sub-branches and other sources of individual variation in vascular supply as shown in classical angiography studies. This vascular parcellation produced smaller displacement error in simulated lesion-symptom analysis compared with individual voxels and Brodmann regions. A second principal component analysis of the patients' detailed neuropsychological data revealed a four-factor solution reflecting phonological, semantic, executive-demand and speech fluency abilities. As a preliminary exploration, stepwise regression was used to relate behavioural factor scores to the lesion principal components. Phonological ability was related to two components, which covered the posterior temporal region including the posterior segment of the arcuate fasciculus, and the inferior frontal gyrus. Three components were linked to semantic ability and were located in the white matter underlying the anterior temporal lobe, the supramarginal gyrus and angular gyrus. Executive-demand related to two components covering the dorsal edge of the middle cerebral artery territory, while speech fluency was linked to two components that were located in the middle frontal gyrus, precentral gyrus and subcortical regions (putamen and thalamus). Future studies can explore in formal terms the utility of these principal component analysis-derived lesion components for relating post-stroke lesions and symptoms.
Project description:Previous lesion behavior studies primarily used univariate lesion behavior mapping techniques to map the anatomical basis of spatial neglect after right brain damage. These studies led to inconsistent results and lively controversies. Given these inconsistencies, the idea of a wide-spread network that might underlie spatial orientation and neglect has been pushed forward. In such case, univariate lesion behavior mapping methods might have been inherently limited in detecting the presumed network due to limited statistical power. By comparing various univariate analyses with multivariate lesion-mapping based on support vector regression, we aimed to validate the network hypothesis directly in a large sample of 203 newly recruited right brain damaged patients. If the exact same correction factors and parameter combinations (FDR correction and dTLVC for lesion size control) were used, both univariate as well as multivariate approaches uncovered the same complex network pattern underlying spatial neglect. At the cortical level, lesion location dominantly affected the temporal cortex and its borders into inferior parietal and occipital cortices. Beyond, frontal and subcortical gray matter regions as well as white matter tracts connecting these regions were affected. Our findings underline the importance of a right network in spatial exploration and attention and specifically in the emergence of the core symptoms of spatial neglect.
Project description:Emerging research suggests spatial neglect after right stroke is linked to dysfunctional attention and motor networks. Advanced functional connectivity analysis clarified brain network recovery, however we need to know how networks participate in adaptive motor performance. We need to verify network changes associated with validated functional measures and spatial-motor performance in spatial neglect, especially in patients with large brain lesions and significant disability. This study tested whether disability-relevant spatial neglect associates with different patterns of resting state functional connectivity between motor, dorsal and ventral attention networks (MN, DAN and VAN). Right stroke patients had spatial neglect (n?=?8) or not (n?=?10) on the Behavioural Inattention Test-conventional. Spatial neglect patients had weaker intranetwork VAN connectivity, and reduced internetwork connectivity between VAN and left frontal eye field (DAN), and between VAN and the left primary motor area (MN). These network impairments might explain the co-occurrence of attention and motor deficits in spatial neglect, and open a path to assessing functional connectivity in clinical trials of combined spatial retraining and motor rehabilitation after stroke.
Project description:Spatial neglect is a neurocognitive disorder that affects perception, representation, and/or motor planning. Neglect dyslexia in spatial neglect after right hemisphere damage may co-occur with, or be dissociated from, other spatial neglect signs. Previous neglect dyslexia research focused on word-level stimuli and reading errors. Using single words for assessment may leave some people with neglect dyslexia undiagnosed, and assessment materials that are closer to texts read in real life may better capture neglect dyslexia.The authors tested reading in 67 right hemisphere stroke survivors with 4 types of text materials: words, phrases, an article, and a menu.Accuracy on reading the menu and article texts was significantly poorer than reading the words and phrases. The hypothesis that assessment materials with ecological validity such as reading a menu and reading an article may be more challenging than reading single words and phrases was supported.Results suggest that neglect dyslexia assessment after stroke should include text materials comparable to those read in everyday life. Increasing the spatial extent of training materials in future research might also yield better functional generalization after right brain stroke.
Project description:A number of conflicting claims have been advanced regarding the role of the left inferior frontal gyrus, inferior parietal lobe and posterior middle temporal gyrus in action recognition, driven in part by an ongoing debate about the capacities of putative mirror systems that match observed and planned actions. We report data from 43 left hemisphere stroke patients in two action recognition tasks in which they heard and saw an action word ('hammering') and selected from two videoclips the one corresponding to the word. In the spatial recognition task, foils contained errors of body posture or movement amplitude/timing. In the semantic recognition task, foils were semantically related (sawing). Participants also performed a comprehension control task requiring matching of the same verbs to objects (hammer). Using regression analyses controlling for both the comprehension control task and lesion volume, we demonstrated that performance in the semantic gesture recognition task was predicted by per cent damage to the posterior temporal lobe, whereas the spatial gesture recognition task was predicted by per cent damage to the inferior parietal lobule. A whole-brain voxel-based lesion symptom-mapping analysis suggested that the semantic and spatial gesture recognition tasks were associated with lesioned voxels in the posterior middle temporal gyrus and inferior parietal lobule, respectively. The posterior middle temporal gyrus appears to serve as a central node in the association of actions and meanings. The inferior parietal lobule, held to be a homologue of the monkey parietal mirror neuron system, is critical for encoding object-related postures and movements, a relatively circumscribed aspect of gesture recognition. The inferior frontal gyrus, on the other hand, was not predictive of performance in any task, suggesting that previous claims regarding its role in action recognition may require refinement.
Project description:Lesion location is an important determinant for post-stroke cognitive impairment. Although several 'strategic' brain regions have previously been identified, a comprehensive map of strategic brain regions for post-stroke cognitive impairment is lacking due to limitations in sample size and methodology. We aimed to determine strategic brain regions for post-stroke cognitive impairment by applying multivariate lesion-symptom mapping in a large cohort of 410 acute ischemic stroke patients. Montreal Cognitive Assessment at three to six months after stroke was used to assess global cognitive functioning and cognitive domains (memory, language, attention, executive and visuospatial function). The relation between infarct location and cognition was assessed in multivariate analyses at the voxel-level and the level of regions of interest using support vector regression. These two assumption-free analyses consistently identified the left angular gyrus, left basal ganglia structures and the white matter around the left basal ganglia as strategic structures for global cognitive impairment after stroke. A strategic network involving several overlapping and domain-specific cortical and subcortical structures was identified for each of the cognitive domains. Future studies should aim to develop even more comprehensive infarct location-based models for post-stroke cognitive impairment through multicenter studies including thousands of patients.