Acute visual neglect and extinction: Distinct functional state of the visuospatial attention system

Department of Neurology, University Medical Centre Freiburg, Freiburg, Germany.
Brain (Impact Factor: 9.2). 09/2011; 134(Pt 11):3310-25. DOI: 10.1093/brain/awr220
Source: PubMed


The neural mechanisms underlying spatial neglect are still disputed. Abnormal left parietal hyperactivation is proposed to lead to the rightward attentional bias, a clinical hallmark of neglect. Extinction, another deficit of visuospatial attention, is regarded as either a 'mild' form of neglect or a distinct syndrome. Although both neglect and extinction are typical syndromes of acute right hemispheric stroke, all imaging studies investigating these syndromes were conducted at least several weeks after stroke onset, in a phase when brain reorganization has already progressed. The present study aimed at comparing the activation patterns in acute stroke patients with neglect and extinction during visuospatial processing. Using functional magnetic resonance imaging, we examined the functional state of the attention system in 33 patients with a first ever stroke (53 ± 5 h after stroke onset) and age-matched healthy subjects (n = 15). All patients had embolic infarcts within the territory of the right middle cerebral artery. Patients were divided into three groups: (i) normal visuospatial processing (control patients, n = 11); (ii) patients with visual extinction but with no signs of neglect (n = 9); and (iii) patients with visual neglect (n = 13). While undergoing functional magnetic resonance imaging, patients performed a Posner-like task for visuospatial attention with detection of the targets in the left and right visual hemifields. Patients with neglect showed the expected imbalance in the left versus right parietal activation, which however, was present also in control and extinction patients, thus representing an epiphenomenon of the acute structural lesion in the right hemisphere. Compared with control patients, neglect was characterized by reduced activation in the right parietal and lateral occipital cortex, as well as in the left frontal eye field. In contrast, the activation pattern in patients with extinction differed from all other groups by an increased activation of the left prefrontal cortex. In both patients with neglect and extinction, detection of targets in the left hemifield correlated with an activation in the left prefrontal and parietal cortex. Thus at least in acute stroke, a relative hyperactivation of the left parietal cortex is not a particular characteristic of neglect. The specific signature of neglect is represented by the dysfunction of the right parietal and lateral occipital cortex. The function of the left attentional centres might provide a compensatory role after critical right hemisphere lesions and be relevant for the contralesional spatial processing.

28 Reads
  • Source
    • "In this respect, we are conscious that a study with healthy participants cannot rule out theories on spatial neglect . However, we believe that the present results, together with the previously described papers with neglect patients, can pose the bases for a further investigation, with neglect patients, on whether hyperactivation of the left hemisphere is causative of spatial neglect, as suggested by the inter-hemispheric rivalry models, or alternatively reflects long-term maladaptive plastic reorganization following a brain lesion, as previous papers (Umarova et al., 2011; Ricci et al., 2012) and the present data seem to suggest. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Spatial neglect is traditionally explained as an imbalance of the interhemispheric reciprocal inhibition exerted by the two hemispheres: after a right lesion, the contralesional hemisphere becomes disinhibited and its enhanced activity suppresses the activity in the lesioned one. Even though the hyperexcitability of the left hemisphere is the theoretical framework of several rehabilitation interventions using non-invasive brain stimulation protocols in neglect, no study has yet investigated directly the actual state of cortical excitability of the contralesional hemisphere immediately after the brain lesion. The present study represents the first attempt to directly assess the interhemispheric rivalry model adopting a novel approach based on the induction of neglect-like biases in healthy participants. Applying repetitive transcranial magnetic stimulation (rTMS) over the right posterior parietal cortex while concurrently recording the EEG activity allows to measure specific neurophysiological markers of cortical activity (i.e. TMS-evoked potentials, TEPs) both over the stimulated right hemisphere and over the contralateral homologous area. Besides the effectiveness of the protocol used in modulating behavior, our results show an inhibition of the cortical excitability of the directly stimulated parietal cortex (right hemisphere) and, most importantly, a comparable reduction of cortical excitability of the homologous contralateral (left) area. TEPs and additional electrophysiological measures reliably provide strong evidence for a bilateral hypo-activation following TMS induction of neglect-like biases. These results suggest that the parietal imbalance typically found in neglect patients could reflect a long-term maladaptive plastic reorganization that follows a brain lesion. Copyright © 2015. Published by Elsevier Ltd.
    Neuropsychologia 04/2015; 72. DOI:10.1016/j.neuropsychologia.2015.04.010 · 3.30 Impact Factor
  • Source
    • "Recent studies found a double dissociation between neglect and extinction, suggesting that these two conditions may reflect separate dysfunctions (Umarova et al., 2011; Vossel et al., 2011; Pavlovskaya, Soroker, & Bonneh, 2007; Bonneh, Pavlovskaya, Ring, & Soroker, 2004; Karnath, Himmelbach, & Küker, 2003; for a review, see de Haan, Karnath, & Driver, 2012). Not all tasks require focused attention. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The syndrome of unilateral spatial neglect (USN) after right-hemisphere damage is characterized by failure of salient left-sided stimuli to activate an orienting response, attract attention, and gain access to conscious awareness. The explicit failure processing left-sided visual information is not uniform, however, and patients seem to be more successful performing certain visual tasks than others. The source of this difference is still not clear. We focus on processing of visual scene statistical properties, asking whether, in computing the average size of an array of objects, USN patients give appropriate weight to objects on the left; disregard left-side objects entirely; or assign them an intermediate, lower weight, in accord with their tendency to neglect these objects. The interest in testing this question stems from a series of studies in healthy individuals that lead Chong and Treisman [Chong, S. C., & Treisman, A. Statistical processing: Computing the average size in perceptual groups. Vision Research, 45, 891-900, 2005a; Chong, S. C., & Treisman, A. Attentional spread in the statistical processing of visual displays. Perception & Psychophysics, 67, 1-13, 2005b] to propose that processing of statistical properties (like the average size of visual scene elements) is carried out in parallel, with no need for serial allocation of focal attention to the different scene elements. Our results corroborate this suggestion, showing that objects in the left ("neglected") hemispace contribute to average size computation, despite a marked imbalance in spatial distribution of attention, which leads to a reduced weight of left-side elements in the averaging computation. This finding sheds light on the nature of the impairment in USN and on basic mechanisms underlying statistical processing in vision. We confirm that statistical processing depends mainly on spread-attention mechanisms, which are largely spared in USN.
    Journal of Cognitive Neuroscience 02/2015; 27(7):1-15. DOI:10.1162/jocn_a_00791 · 4.09 Impact Factor
  • Source
    • "Based on our previous studies on small samples of stroke patients, we have proposed that specialized dorsal fronto-parietal regions, despite their structural integrity, exhibit in neglect patients abnormal interhemispheric task-evoked responses (Corbetta et al., 2005; cf. Umarova et al., 2011 for opposite findings) and resting state functional connectivity (He et al., 2007; Carter et al., 2010); moreover, these dysfunctions correlate with the severity of neglect (Corbetta et al., 2005; He et al., 2007; Carter et al., 2010). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The relationship between spontaneous brain activity and behaviour following focal injury is not well understood. Here, we report a large-scale study of resting state functional connectivity MRI and spatial neglect following stroke in a large (n = 84) heterogeneous sample of first-ever stroke patients (within 1-2 weeks). Spatial neglect, which is typically more severe after right than left hemisphere injury, includes deficits of spatial attention and motor actions contralateral to the lesion, and low general attention due to impaired vigilance/arousal. Patients underwent structural and resting state functional MRI scans, and spatial neglect was measured using the Posner spatial cueing task, and Mesulam and Behavioural Inattention Test cancellation tests. A principal component analysis of the behavioural tests revealed a main factor accounting for 34% of variance that captured three correlated behavioural deficits: visual neglect of the contralesional visual field, visuomotor neglect of the contralesional field, and low overall performance. In an independent sample (21 healthy subjects), we defined 10 resting state networks consisting of 169 brain regions: visual-fovea and visual-periphery, sensory-motor, auditory, dorsal attention, ventral attention, language, fronto-parietal control, cingulo-opercular control, and default mode. We correlated the neglect factor score with the strength of resting state functional connectivity within and across the 10 resting state networks. All damaged brain voxels were removed from the functional connectivity:behaviour correlational analysis. We found that the correlated behavioural deficits summarized by the factor score were associated with correlated multi-network patterns of abnormal functional connectivity involving large swaths of cortex. Specifically, dorsal attention and sensory-motor networks showed: (i) reduced interhemispheric functional connectivity; (ii) reduced anti-correlation with fronto-parietal and default mode networks in the right hemisphere; and (iii) increased intrahemispheric connectivity with the basal ganglia. These patterns of functional connectivity:behaviour correlations were stronger in patients with right- as compared to left-hemisphere damage and were independent of lesion volume. Our findings identify large-scale changes in resting state network interactions that are a physiological signature of spatial neglect and may relate to its right hemisphere lateralization.
    Brain 11/2014; 137(12). DOI:10.1093/brain/awu297 · 9.20 Impact Factor
Show more