Abstract
Visual neglect after left-hemispheric lesion is thought to be less frequent, less severe, and shorter lived than visuospatial attention deficits resulting from right-hemispheric lesions. However, reports exist opposing this assumption, and it is unclear how these findings fit into the current theories of visuospatial processing. Furthermore, only little is known about the exact structure–function relationship between visuospatial attention deficits and left-hemispheric stroke. We investigated neglect in 121 patients with acute left-hemispheric ischemic stroke by following clinical development from within the first 24 h of stroke onset until hospital discharge. Visuospatial attention deficits occurred in 17.4 % (n = 21). Voxel-based lesion–symptom mapping associated visual neglect to the right with lesion in the left superior and middle temporal gyrus, temporal pole, frontal operculum, and insula. Neglect severity, captured by the Center of Cancellation Score of the Bells test, was associated with lesion in the left anterior temporal lobe and the left frontal operculum. The left-hemispheric lesion pattern of neglect thus involves areas of the ventral attention system and partly mirrors the critical regions of the right hemisphere known to be associated with neglect. Based on our prospective analysis on a large cohort of patients with left-hemispheric stroke, this study shows that in a remarkable number of patients, the left hemisphere essentially contributes to an intact representation of space and clarifies the impact of the distinct left-hemispheric structures involved in visuospatial processing.
Similar content being viewed by others
References
Albert ML (1973) A simple test of visual neglect. Neurology 23:658–664
Alexander MP, Annett M (1996) Crossed aphasia and related anomalies of cerebral organization: case reports and a genetic hypothesis. Brain Lang 55(2):213–239
Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113
Azouvi P, Samuel C, Louis-Dreyfus A, Bernati T, Bartolomeo P, Beis JM et al (2002) Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. J Neurol Neurosurg Psychiatry 73(2):160–166
Bartolo A, Cubelli R, Della Sala S (2008) Cognitive approach to the assessment of limb apraxia. Clin Neuropsychol 21:27–45
Becker E, Karnath HO (2007) Incidence of visual extinction after left versus right hemisphere stroke. Stroke 38(12):3172–3174
Beis JM, Keller C, Morin N, Bartolomeo P, Bernati T, Chokron S et al (2005) Right spatial neglect after left hemisphere stroke: qualitative and quantitative study. Neurology 63:1600–1605
Beume LA, Kaller CP, Hoeren M, Klöppel S, Kuemmerer D, Glauche V et al (2015) Processing of bilateral versus unilateral conditions: evidence for the functional contribution of the ventral attention network. Cortex 66:91–102
Binder J, Marshall R, Lazar R, Benjamin J, Mohr JP (1992) Distinct syndromes of hemineglect. Arch Neurol 49:1187–1194
Bisiach E (1991) Extinction and neglect: same or different? In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 251–257
Blini E, Romeo Z, Spironelli C, Pitteri M, Meneghello F, Bonato M et al (2016) Multi-tasking unconvers right spatial neglect and extinction in chronic left-hemispheric stroke patients. Brain Connect. doi:10.1016/j.neuropsychologia.2016.02.028
Bowen A, McKenna K, Tallis RC (1999) Reasons for variability in the reported rate of occurrence of unilateral spatial neglect after stroke. Stroke 30:1196–1202
Brunner E, Munzel U (2000) The nonparametric Behrens-fisher problem: asymptotic theory and a small-sample approximation. Biom J 42(1):17–25
Bushman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860
Buxbaum LJ, Ferraro MK, Veramonti T, Farne A, Whyte J, Ladavas E, Frassinetti F, Coslett HB (2004) Hemispatial neglect: subtypes, neuroanatomy and disability. Neurology 62(5):749–756
Cabeza R (2002) Hemispheric asymmetry reduction in old adults: the HAROLD model. Psychol Aging 17:85–100
Carr MS, Jacobson T, Boller F (1981) Crossed aphasia: analysis of four cases. Brain Lang 14:190–202
Cassidy TP, Lewis S, Gray CS (1998) Recovery from visuospatial neglect in stroke patients. J Neurol Neurosurg Psychiatry 64(4):555–557
Chance SA, Crow TJ (2007) Distinctively human: cerebral lateralisation and language in Homo sapiens. J Anthropol Sci 85:83–100
Chechlacz M, Rotshtein P, Bickerton WL, Hansen PC, Deb S, Humphreys GW (2001) Separating neural correlates of allocentric and egocentric neglect: distinct cortical sites and common white matter disconnections. Cogn Neuropsychol 27(3):277–303
Cocchini G, Cubelli R, Della Sala S, Beschin N (1999) Neglect without extinction. Cortex 35:285–313
Committeri G, Pitzalis S, Galati G, Patria F, Pelle G, Sabatini U et al (2007) Neural bases of personal and extrapersonal neglect in humans. Brain 130:431–441
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Corbetta M, Shulman GL (2011) Spatial neglect and attention networks. Annu Rev Neurosci 34:569–599
Corbetta M, Kincade MJ, Lewis C, Snyder AZ, Sapir A (2005) Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci 8(11):1603–1610
Corbetta M, Ramsey L, Callejas A, Baldassarre A, Hacker CD, Siegel JS et al (2015) Common behavioral clusters and subcortial anatomy in stroke. Neuron 85(5):927–941
Costa LD, Vaughan HG Jr, Horwitz M, Ritter W (1969) Patterns of behavioral deficit associated with visual spatial neglect. Cortex 5:242–263
Denes G, Semenza C, Stoppa E, Lis A (1982) Unilateral spatial neglect and recovery from hemiplegia. Brain 105:543–552
Engelter ST, Gostynski M, Papa S, Frei M, Born C, Ajdacic-Gross V et al (2006) Epidemiology of aphasia attributable to first ischemic stroke: incidence, severity, fluency, etiology, thrombolysis. Stroke 37(6):1379–1384
Farne A, Buxbaum LJ, Ferraro M, Frassinetti F, Whyte J, Veramonti T et al (2004) Patterns of spontaneous recovery of neglect and associated disorders in acute right brain-damaged patients. J Neurol Neurosurg Psychiatry 75(10):1401–1410
Fels M, Geissner E (1997) Neglect-test (NET) Ein Verfahren zur Erfassung visueller Neglectphänomene. Hogrefe, Göttingen
Ferber S, Karnath HO (2001) How to assess spatial neglect: line bisection or cancellation takss? J Clin Exp Neuropsychol 23(5):599–607
Fullerton KJ, McSherry D, Stout RW (1986) Albert’s test: a neglected test of perceptual neglect. Lancet 1(8476):430–432
Gainotti G (1968) Les manifestations de negligence et d’inattention pour l’hemispace. Cortex 4:64–91
Gauthier L, Dehaut F, Joanette Y (1989) The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 11:49–54
Golay L, Schnider A, Ptak R (2008) Cortical and subcortical anatomy of chronic spatial neglect following vascular damage. Behav Brain Funct 4:43
Goldenberg G, Karnath H (2006) The neural basis of imitation is body part specific. J Neurosci 26:6282–6287
Halligan PW, Marshall JC, Wade DT (1989) Visuospatial neglect: underlying factors and test sensitivity. Lancet 2(8668):908–911
Hartwigsen G, Price CJ, Baumgaertner A, Geiss G, Koehnke M, Ulmer S, Siebner HR (2010) The right posterior inferior frontal gyrus contributes to phonological word decisions in the healthy brain: evidence from dual-site TMS. Neuropsychologia 48(10):3155–3163
Hécaen H, Mazars G, Ramier AM, Goldblum MC, Mérienne L (1971) L’aphasie croisée chez un subjet bilingue (vietnamien-francais). Rev Neurol 124:319–323
Heilman KM, Valenstein E (1972) Frontal lobe neglect in man. Neurology 21:660–664
Heilman KM, Valenstein E (1979) Mechanisms underlying hemispatial neglect. Ann Neurol 5:166–170
Heilman KM, Van Den Abell T (1980) Right hemisphere dominance for attention: the mechanism underlying hemispheric asymmetries of inattention. Neurology 30(3):327–330
Heilman KM, Watson RT (2011) Neglect and related disorders. In: Heilman KM, Valenstein E (eds) Clinical neuropsychology. OUP, New York, pp 243–293
Hellige JB (1990) Hemispheric asymmetry. Annu Rev Psychol 41:55–80
Hillis AE, Newhart M, Heidler J, Barker PB, Herskovits E, Degoankar M (2005) Anatomy of spatial attention: insights from perfusion imaging and hemispatial neglect in acute stroke. J Neurosci 25:3161–3167
Himmelbach M, Erb M, Karnath O (2006) Exploring the visual world: the neural substrate of spatial orienting. Neuroimage 32(4):1747–1759
Hoeren M, Kaller CP, Glauche V, Vry MS, Rijntjes M, Hamzei F et al (2013) Action semantics and movement characteristics engage distinct processing streams during the observation of tool use. Exp Brain Res 229(2):243–260
Hoeren M, Kümmerer D, Bormann T, Beume L, Ludwig VM, Vry MS, Mader I, Rijntjes M, Kaller CP, Weiller C (2014) Neural bases of imitation and pantomime in acute stroke patients: distinct streams for praxis. Brain 137(10):2796–2810
Huber W, Poeck K, Willmes K (1984) The Aachen Aphasia Test. Adv Neurol 41:291–303
Husain M, Kennard C (1997) Distractor-dependent frontal neglect. Neuropsychologia 35:829–841
Ihori N, Kashiwagi A, Kashiwagi T (2015) Right unilateral spatial neglect in aphasic patients. Brain Lang 147:21–29
Joanette Y, Puel M, Nespoulous JL, Rascol A, Lecours AR (1982) Aphasie croisée chez les droitiers. Rev Neurol 138:575–586
Kamtchum Tatuene J, Allali G, Saj A, Bernati T, Sztajzel R, Pollak P et al (2016) Incidence, risk factors and anatomy of peripersonal visuospatial neglect in acute stroke. Eur Neurol 75(3–4):157–163
Kanwisher N, Woicuulik E (2000) Visual attention: insights form brain imaging. Nat Rev Neurosci 1:91–100
Karnath HO, Rorden C (2012) The anatomy of spatial neglect. Neuropsychologia 50:1010–1017
Karnath HO, Ferber S, Himmelbach M (2001) Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411(6840):950–953
Karnath HO, Himmelbach M, Küker W (2003) The cortical substrate of visual extinction. NeuroReport 14(3):437–442
Karnath HO, Fruhmann Berger M, Küker W, Rorden C (2004) The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14:1164–1172
Karnath HO, Rorden C, Ticini LF (2009) Damage to white matter fiber tracts in acute spatial neglect. Cereb Cortex 19(10):2331–2337
Karnath HO, Rennig J, Johannsen L, Rorden C (2011) The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain 134(Pt 3):903–912
Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341
Klein E, Moeller K, Glauche V, Weiller C, Willmes K (2013) Processing pathways in mental arithmetic: evidence from probabilistic fibre tracking. PLoS ONE 8(1):e55455
Kleinman JT, Newhart M, Davis C, Heidler-Gary J, Gottesman RF, Hillis AE (2007) Right hemispatial neglect: frequency and characterization following acute left hemispheric stroke. Brain Cogn 64(1):50–59
Kuemmerer D, Hartwigsen G, Kellmeyer P, Glauche V, Mader I, Klöppel S et al (2013) Damage to ventral and dorsal language pathways in acute aphasia. Brain 136(2):619–629
Laska AC, Hellblom A, Murray V, Kahan T, Von Arbin M (2001) Aphasia in acute stroke and relation to outcome. J Intern Med 249(5):413–422
Liebermeister C (1877) Über Wahrscheinlichkeitsrechnung in Anwendung auf therapeutische Statistik. Sammlung Klinischer Vorträge 110:935–962
Machner B, Dorr M, Sprenger A, von der Gablentz J, Heide W, Barth E, Helmchen C (2012) Impact of dynamic bottom-up features and top-down control on the visual exploration of moving real-world scenes in hemispatial neglect. Neuropsychologia 50(10):2415–2425
Maeshima S, Shigeno K, Dohi N, Kajiwara T, Komai N (1992) A study of right unilateral spatial neglect in left hemispheric lesions: the difference between right-handed and non-right-handed post-stroke patients. Acta Neurol Scand 85(6):418–424
Marsh E, Hillis AE (2008) Dissociation between egocentric and allocentric visuospatial and tactile neglect in acute stroke. Cortex 44(9):1215–1250
Martin M, Beume L, Kuemmerer D, Schmidt CS, Bormann T, Dressing A et al (2015) Differential roles of ventral and dorsal streams for conceptual and production-related components of tool use in acute stroke patients. Cereb Cortex 26(9):3754–3771
Mattingley JB, Bradshaw JL (1994) How many neglects? Some considerations based on anatomy and information processing. Neuropsychol Rehabil 4:169–172
Medina J, Kimberg DY, Chatterjee A, Coslett HB (2010) Inappropriate usage of the Brunner–Munzel test in recent voxel-based lesion-symptom mapping studies. Neuropsychologia 48(1):341–343
Mesulam MM (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10(4):309–325
Mesulam MM (1999) Spatial attention and neglect: parietal, frontal and cingulated contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc B Biol Sci 354:1325–1346
Milner AD (1997) Neglect, extinction and the cortical streams of visual processing. In: Thier P, Karnath HO (eds) Parietal lobe contributions to orientation in 3D space. Springer, Heidelberg, pp 3–22
Molenberghs P, Sale MV (2011) Testing for spatial neglect with line bisection and target cancellation: are both tasks really unrelated? PLoS ONE 6(7):e23017
Mort DJ, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, Husain M (2003) The anatomy of visual neglect. Brain 126:1986–1997
Ogden JA (1985) Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect. Brain Cogn 4:59–75
Ogden JA (1987) The ‘neglected’ left hemisphere and its contribution to visuospatial neglect. In: Jeannerod M (ed) Neurophysiological and neuropsychological aspects of spatial neglect. Elsevier Science Publishers, North Holland, pp 215–233
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 8:97–113
Oleksiak A, Postma A, van der Ham IJ, Klink PC, van Wezel RJ (2011) A review of lateralization of spatial functioning in nonhuman primates. Brain Res Rev 67(1–2):56–72
Ota H, Fuji T, Suzuki K, Fukatsu R, Yamadori A (2001) Dissociation of body-centered and stimulus centered representations in unilateral neglect. Neurology 57:2064–2069
Pedersen PM, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS (1995) Aphasia in acute stroke: incidence, determinants, recovery. Ann Neurol 38(4):659–666
Pedersen P, Jorgensen H, Nakayama H, Raaschou H, Olsen T (1997) Hemineglect in acute stroke-incidence and prognostic implications: the Copenhagen Stroke Study. Am J Phys Med Rehabil 76(2):122–127
Previc FH (1991) A general theory concerning the prenatal origins of cerebral lateralization in humans. Psychol Rev 98(3):299–334
Rengachary J, He BJ, Shulman GL, Corbetta M (2011) A behavioral analysis of spatial neglect and its recovery after stroke. Front Hum Neurosci 45:29
Rijntjes M, Weiller C, Bormann T, Musso M (2013) The dual loop model: its relation to language and other modalities. Front Evol Neurosci 4:9
Ringman JM, Saver JL, Woolson RF, Clarke WR, Adams HP (2004) Frequency, risk factors, anatomy, course of unilateral neglect in an acute stroke cohort. Neurology 63(3):468–474
Robertson I, Marshall J (1993) Unilateral neglect. Clinical and experimental studies. Lawrence Erlbaum Associates, Hove
Rorden C, Karnath HO (2010) A simple measure of neglect severity. Neuropsychologia 48(9):2758–2763
Rorden C, Fruhmann Berger M, Karnath HO (2006) Disturbed line bisection is associated with posterior brain lesions. Brain Res 1080(1):17–25
Saj A, Verdon V, Vocat R, Vuilleumier P (2012) ‘The anatomy underlying acute versus chronic spatial neglect’ also depends on clinical tests. Brain 135(Pt2):e207
Smith DV, Clithero JA, Rorden C, Karnath HO (2013) Decoding the anatomical network of spatial attention. Proc Natl Acad Sci 110(4):1518–1523
Sperber C, Karnath HO (2016) Diagnostic validity of line bisection in the acute phase of stroke. Neuropsychologia 82:200–204
Stone SP, Wilson B, Wroot A, Halligan PW, Lange LS, Marshall JC, Greenwood RJ (1991) The assessment of visuospatial neglect after acute stroke. J Neurol Neurosurg Psychiatry 54:345–350
Stone SP, Halligan PW, Greenwood RJ (1993) The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age Ageing 21:48–52
Suchan J, Karnath HO (2011) Spatial orienting by left hemisphere language areas: a relic from the past? Brain 134:3059–3070
Suchan J, Rorden C, Karnath HO (2012) Neglect severity after left and right brain damage. Neuropsychologia 50:1136–1141
Sunderland A, Wade DT, Langton-Hewer R (1987) The natural history of visual neglect after stroke: indications from two methods of assessment. J Int Disabil Stud 8:55–59
Taylor D, Ashburn A, Ward CD (1994) Asymmetrical trunk posture, unilateral neglect and motor performance following stroke. Clin Rehabil 8:48–53
Umarova RM, Saur D, Kaller CP, Vry MS, Glauche V, Mader I et al (2011) Acute visual neglect and extinction: distinct functional state of the visuospatial attention system. Brain 134(11):3310–3325
Vallar G, Perani D (1986) The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man. Neuropsychologia 24:609–622
Vallar G, Rusconi ML, Geminiani G, Berti A, Cappa SF (1991) Visual and nonvisual neglect after unilateral brain lesions: modulation by visual input. Int J Neurosci 61(3–4):229–239
Vallar G, Rusconi ML, Bignamini L, Geminiani G, Perani D (1994) Anatomical correlates of visual and tactile extinction in humans: a clinical CT scan study. J Neurol Neurosurg Psychiatry 57(4):464–470
Vandervliet EJ, Verhoeven J, Engelborghs S, De Deyn PP, Parizel PM, Marien P (2008) FMRI findings in an aphasic patient with reversed cerebral dominance for language. Acta Neurol Belg 108(4):161–166
Verdon V, Schwartz S, Loyblad KO, Hauert CA, Vuilleumier P (2010) Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain 133(3):880–894
Weiller C, Isensee C, Rijntjes M, Huber W, Müller S, Bier D, Dutschka K, Woods RP, Noth J, Diener HC (1995) Recovery from Wernicke’s aphasia: a positron emission tomographic study. Ann Neurol 37(6):723–732
Weiller C, Musso M, Rijntjes M, Saur D (2009) Please don’t underestimate the ventral pathway in language. Trends Cogn Sci 13(9):369–370
Weiller C, Bormann T, Saur D, Musso M, Rijntjes M (2011) How the ventral pathway got lost: and what its recovery might mean. Brain Lang 118(1–2):29–39
Wilson B, Cockburn J, Haligan PW (1987) Behavioural inattention test. Thames Valley Company, Titchfield
Acknowledgments
We thank G. Lind, S. Hoefer, S. Karn, and H. Mast for assistance in data acquisition and K. Astrahantseff for manuscript editing.
Funding
None of the authors has any financial or personal relationships with individuals or organizations that could inappropriately influence this submission. This work was supported by the Brain Links—Brain Tools Cluster of Excellence funded by the German Research Foundation (DFG, Grant #EXC1086).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Beume, LA., Martin, M., Kaller, C.P. et al. Visual neglect after left-hemispheric lesions: a voxel-based lesion–symptom mapping study in 121 acute stroke patients. Exp Brain Res 235, 83–95 (2017). https://doi.org/10.1007/s00221-016-4771-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4771-9