Abstract
Spatial neglect usually concerns left-sided events after right-hemisphere damage. Its anatomical correlates are debated, with evidence suggesting an important role for fronto-parietal white matter disconnections in the right hemisphere. Here, we describe the less frequent occurrence of neglect for right-sided events, observed in three right-handed patients after a focal stroke in the left hemisphere. Patients were tested 1 month and 3 months after stroke. They performed a standardized paper-and-pencil neglect battery and underwent brain MRI with both structural and diffusion tensor (DT) sequences, in order to assess both grey matter and white matter tracts metrics. Lesions were manually reconstructed for each patient. Patients presented signs of mild right-sided neglect during visual search and line bisection. One patient also showed pathological performance in everyday life. Structural MRI demonstrated left parietal strokes in two patients, in the region extending from the postcentral gyrus to the temporo-parietal junction. One of these two patients also had had a previous occipital stroke. The remaining patient had a left frontal stroke, affecting the precentral, the postcentral gyri and the basal ganglia. DT MRI tractography showed disconnections in the fronto-parietal regions, concerning principally the superior longitudinal fasciculus (SLF). These results suggest an important role for left SLF disconnection in right-side neglect, which complements analogous evidence for right SLF disconnection in left-side neglect.
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References
Albert ML (1973) A simple test of visual neglect. Neurology 23(6):658–664
Andrade K, Samri D, Sarazin M, de Souza LC, Cohen L, Thiebaut de Schotten M et al (2010) Visual neglect in posterior cortical atrophy. BMC Neurol 10:68. https://doi.org/10.1186/1471-2377-10-68
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
Azouvi P, Bartolomeo P, Beis J-M, Perennou D, Pradat-Diehl P, Rousseaux M (2006) A battery of tests for the quantitative assessment of unilateral neglect. Restor Neurol Neurosci 24(4–6):273–285
Bartolomeo P (2019) Visual neglect: getting the hemispheres to talk to each other. Brain 142(4):840–842. https://doi.org/10.1093/brain/awz043
Bartolomeo P (2021) From competition to cooperation: visual neglect across the hemispheres. Rev Neurol 177(9):1104–1111. https://doi.org/10.1016/j.neurol.2021.07.015
Bartolomeo P, Thiebaut de Schotten M (2016) Let thy left brain know what thy right brain doeth: inter-hemispheric compensation of functional deficits after brain damage. Neuropsychologia 93(Pt B):407–412. https://doi.org/10.1016/j.neuropsychologia.2016.06.016
Bartolomeo P, Seidel Malkinson T (2019) Hemispheric lateralization of attention processes in the human brain. Curr Opin Psychol 29:90–96. https://doi.org/10.1016/j.copsyc.2018.12.023
Bartolomeo P, Dalla Barba G, Boisse MF, Bachoud-Levi AC, Degos JD, Boller F (1998) Right-side neglect in Alzheimer’s disease. Neurology 51(4):1207–1209
Bartolomeo P, Thiebaut de Schotten M, Doricchi F (2007) Left unilateral neglect as a disconnection syndrome. Cereb Cortex 17(11):2479–2490
Bartolomeo P, Thiebaut de Schotten M, Chica AB (2012) Brain networks of visuospatial attention and their disruption in visual neglect. Front Hum Neurosci 6:110. https://doi.org/10.3389/fnhum.2012.00110
Batrancourt B, Levy R, Lehericy S, Hasboun D, Samson Y, Lavallee I et al (2002) An anatomofunctional brain database. C R Biol 325(4):439–455. https://doi.org/10.1016/s1631-0691(02)01444-0
Beis JM, Keller C, Morin N, Bartolomeo P, Bernati T, Chokron S et al (2004) Right spatial neglect after left hemisphere stroke: qualitative and quantitative study. Neurology 63(9):1600–1605
Beume LA, Martin M, Kaller CP, Kloppel S, Schmidt CS, Urbach H et al (2017) Visual neglect after left-hemispheric lesions: a voxel-based lesion-symptom mapping study in 121 acute stroke patients. Exp Brain Res 235(1):83–95. https://doi.org/10.1007/s00221-016-4771-9
Beume LA, Rijntjes M, Dressing A, Kaller CP, Hieber M, Martin M et al (2020) Dissociation of visual extinction and neglect in the left hemisphere. Cortex 129:211–222. https://doi.org/10.1016/j.cortex.2020.04.010
Bowen A, McKenna K, Tallis RC (1999) Reasons for variability in the reported rate of occurrence of unilateral spatial neglect after stroke. Stroke 30(6):1196–1202
Cambier J, Masson M, Guillot M, Robine B (1985) Right neglect with hemiasomatognosia, mental confusion, apraxia and agraphia without aphasia. Rev Neurol 141(12):802–805
Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132. https://doi.org/10.1016/j.cortex.2008.05.004
Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16. https://doi.org/10.1002/ana.20319
Cazzoli D, Muri RM, Schumacher R, von Arx S, Chaves S, Gutbrod K et al (2012) Theta burst stimulation reduces disability during the activities of daily living in spatial neglect. Brain 135(Pt 11):3426–3439. https://doi.org/10.1093/brain/aws182
Charras P, Herbet G, Deverdun J, de Champfleur NM, Duffau H, Bartolomeo P, Bonnetblanc F (2015) Functional reorganization of the attentional networks in low-grade glioma patients: a longitudinal study. Cortex 63:27–41. https://doi.org/10.1016/j.cortex.2014.08.010
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215. https://doi.org/10.1038/nrn755
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. https://doi.org/10.1038/nn1574
D’Erme P, De Bonis C, Gainotti G (1987) Influenza dell’emi-inattenzione e dell’emianopsia sui compiti di bisezione di linee nei pazienti cerebrolesi [Influence of unilateral neglect and hemianopia on line bisection performance in brain-damaged patients]. Arch Psicol Neurol Psichiatr 48:165–189
Doricchi F, Thiebaut de Schotten M, Tomaiuolo F, Bartolomeo P (2008) White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex 44(8):983–995. https://doi.org/10.1016/j.cortex.2008.03.006
Fischer RS, Alexander MP, Gabriel C, Gould E, Milione J (1991) Reversed lateralization of cognitive functions in right handers. Exceptions to classical aphasiology. Brain 114(Pt 1A):245–261
Gainotti G, Tiacci C (1971) The relationships between disorders of visual perception and unilateral spatial neglect. Neuropsychologia 9:451–458
Gainotti G, D’Erme P, Monteleone D, Silveri MC (1986) Mechanisms of unilateral spatial neglect in relation to laterality of cerebral lesions. Brain 109(Pt 4):599–612
Gainotti G, D’Erme P, Bartolomeo P (1991) Early orientation of attention toward the half space ipsilateral to the lesion in patients with unilateral brain damage. J Neurol Neurosurg Psychiatry 54(12):1082–1089
Gauthier L, Dehaut F, Joanette Y (1989) The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 11:49–53
Heilman KM, Watson RT, Valenstein E (1993) Neglect and related disorders. In: Heilman KM, Valenstein E (eds) Clinical neuropsychology, 3rd edn. Oxford University Press, New York, pp 279–336
https://scholar.google.ca/scholar?cluster=8793522007616707829h&hl=en&as_sdt=0,5&sciodt=0,5
Kinsbourne M (1977) Hemi-neglect and hemisphere rivalry. In: Weinstein EA, Friedland RP (eds) Hemi-inattention and hemisphere specialization, vol 18. Raven Press, New York, pp 41–49
Knecht S, Floel A, Drager B, Breitenstein C, Sommer J, Henningsen H et al (2002) Degree of language lateralization determines susceptibility to unilateral brain lesions. Nat Neurosci 5(7):695–699. https://doi.org/10.1038/nn868
Koch G, Oliveri M, Cheeran B, Ruge D, Lo Gerfo E, Salerno S et al (2008) Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain 131(Pt 12):3147–3155. https://doi.org/10.1093/brain/awn273
Koch G, Bonni S, Giacobbe V, Bucchi G, Basile B, Lupo F et al (2012) Theta-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology 78(1):24–30. https://doi.org/10.1212/WNL.0b013e31823ed08f
Lunven M, Thiebaut de Schotten M, Bourlon C, Duret C, Migliaccio R, Rode G, Bartolomeo P (2015) White matter lesional predictors of chronic visual neglect: a longitudinal study. Brain 138(Pt 3):746–760. https://doi.org/10.1093/brain/awu389
Lunven M, Rode G, Bourlon C, Duret C, Migliaccio R, Chevrillon E et al (2019) Anatomical predictors of successful prism adaptation in chronic visual neglect. Cortex 120:629–641. https://doi.org/10.1016/j.cortex.2018.12.004
Malherbe C, Umarova RM, Zavaglia M, Kaller CP, Beume L, Thomalla G et al (2018) Neural correlates of visuospatial bias in patients with left hemisphere stroke: a causal functional contribution analysis based on game theory. Neuropsychologia 115:142–153. https://doi.org/10.1016/j.neuropsychologia.2017.10.013
Mark VW, Kooistra CA, Heilman KM (1988) Hemispatial neglect affected by non-neglected stimuli. Neurology 38(8):1207–1211
Mesulam MM (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10(4):309–325. https://doi.org/10.1002/ana.410100402
Mesulam MM (1985) Principles of behavioral neurology. F.A. Davis, Philadelphia
Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28(5):597–613. https://doi.org/10.1002/ana.410280502
Mesulam MM (1999) Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci 354(1387):1325–1346. https://doi.org/10.1098/rstb.1999.0482
Migliaccio R, Agosta F, Scola E, Magnani G, Cappa SF, Pagani E et al (2012a) Ventral and dorsal visual streams in posterior cortical atrophy: a DT MRI study. Neurobiol Aging 33(11):2572–2584. https://doi.org/10.1016/j.neurobiolaging.2011.12.025
Migliaccio R, Agosta F, Toba MN, Samri D, Corlier F, de Souza LC et al (2012b) Brain networks in posterior cortical atrophy: a single case tractography study and literature review. Cortex 48(10):1298–1309. https://doi.org/10.1016/j.cortex.2011.10.002
Moore MJ, Gillebert CR, Demeyere N (2021) Right and left neglect are not anatomically homologous: a voxel-lesion symptom mapping study. Neuropsychologia 162:108024. https://doi.org/10.1016/j.neuropsychologia.2021.108024
Nyffeler T, Vanbellingen T, Kaufmann BC, Pflugshaupt T, Bauer D, Frey J et al (2019) Theta burst stimulation in neglect after stroke: functional outcome and response variability origins. Brain 142(4):992–1008. https://doi.org/10.1093/brain/awz029
Ogden JA (1985) Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect. Brain Cogn 4(1):59–75
Posner MI, Walker JA, Friedrich FJ, Rafal RD (1984) Effects of parietal injury on covert orienting of attention. J Neurosci 4:1863–1874
Rastelli F, Funes MJ, Lupiáñez J, Duret C, Bartolomeo P (2008) Left neglect: is the disengage deficit space- or object-based? Exp Brain Res 187(3):439–446
Schenkenberg T, Bradford DC, Ajax ET (1980) Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology 30(5):509–517
Siéroff E, Decaix C, Chokron S, Bartolomeo P (2007) Impaired orienting of attention in left unilateral neglect: A componential analysis. Neuropsychology 21(1):94–113. https://doi.org/10.1037/0894-4105.21.1.94
Stengel C, Sanches C, Toba MN, Valero-Cabre A (2022) Things you wanted to know (but might have been afraid to ask) about how and why to explore and modulate brain plasticity with non-invasive neurostimulation technologies. Rev Neurol. https://doi.org/10.1016/j.neurol.2021.12.014
Stone SP, Wilson B, Wroot A, Halligan PW, Lange LS, Marshall JC, Greenwood RJ (1991) The assessment of visuo-spatial neglect after acute stroke. J Neurol Neurosurg Psychiatry 54(4):345–350
Stone SP, Patel P, Greenwood RJ, Halligan PW (1992) Measuring visual neglect in acute stroke and predicting its recovery: the visual neglect recovery index. J Neurol Neurosurg Psychiatry 55(6):431–436
Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309(5744):2226–2228. https://doi.org/10.1126/science.1116251
Thiebaut de Schotten M, Kinkingnehun S, Delmaire C, Lehericy S, Duffau H, Thivard L et al (2008) Visualization of disconnection syndromes in humans. Cortex 44(8):1097–1103. https://doi.org/10.1016/j.cortex.2008.02.003
Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246. https://doi.org/10.1038/nn.2905
Thiebaut de Schotten M, Tomaiuolo F, Aiello M, Merola S, Silvetti M, Lecce F et al (2014) Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual “in vivo” tractography dissection. Cereb Cortex 24(3):691–706. https://doi.org/10.1093/cercor/bhs351
Toba MN, Barbeau EJ (2021) Plasticity and cerebral reorganization: an update. Rev Neurol 177(9):1090–1092. https://doi.org/10.1016/j.neurol.2021.10.001
Toba MN, Zavaglia M, Rastelli F, Valabregue R, Pradat-Diehl P, Valero-Cabre A, Hilgetag CC (2017) Game theoretical mapping of causal interactions underlying visuo-spatial attention in the human brain based on stroke lesions. Hum Brain Mapp. https://doi.org/10.1002/hbm.23601
Toba MN, Migliaccio R, Batrancourt B, Bourlon C, Duret C, Pradat-Diehl P et al (2018a) Common brain networks for distinct deficits in visual neglect. A combined structural and tractography MRI approach. Neuropsychologia 115:167–178. https://doi.org/10.1016/j.neuropsychologia.2017.10.018
Toba MN, Rabuffetti M, Duret C, Pradat-Diehl P, Gainotti G, Bartolomeo P (2018b) Component deficits of visual neglect: “magnetic” attraction of attention vs. impaired spatial working memory. Neuropsychologia 109:52–62. https://doi.org/10.1016/j.neuropsychologia.2017.11.034
Toba MN, Godefroy O, Rushmore RJ, Zavaglia M, Maatoug R, Hilgetag CC, Valero-Cabré A (2020a) Revisiting “brain modes” in a new computational era: approaches for the characterization of brain-behavioural associations. Brain 143(4):1088–1098. https://doi.org/10.1093/brain/awz343
Toba MN, Malherbe C, Godefroy O, Rushmore RJ, Zavaglia M, Maatoug R et al (2020b) Reply: inhibition between human brain areas or methodological artefact? Brain 143(5):e39. https://doi.org/10.1093/brain/awaa093
Toba MN, Zavaglia M, Malherbe C, Moreau T, Rastelli F, Kaglik A et al (2020c) Game theoretical mapping of white matter contributions to visuospatial attention in stroke patients with hemineglect. Hum Brain Mapp 41(11):2926–2950. https://doi.org/10.1002/hbm.24987
Toba MN, Pagliari C, Rabuffetti M, Nighoghossian N, Rode G, Cotton F et al (2021) Quantitative assessment of motor neglect. Stroke 52(5):1618–1627. https://doi.org/10.1161/STROKEAHA.120.031949
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289. https://doi.org/10.1006/nimg.2001.0978
Urbanski M, Thiebaut de Schotten M, Rodrigo S, Oppenheim C, Touze E, Meder JF et al (2011) DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res 208(4):491–505. https://doi.org/10.1007/s00221-010-2496-8
Valero-Cabré A, Toba MN, Hilgetag CC, Rushmore RJ (2020) Perturbation-driven paradoxical facilitation of visuo-spatial function: revisiting the 'Sprague effect'. Cortex 122:10–39. https://doi.org/10.1016/j.cortex.2019.01.031
Vuilleumier P, Hester D, Assal G, Regli F (1996) Unilateral spatial neglect recovery after sequential strokes. Neurology 46(1):184–189
Weintraub S, Daffner KR, Ahern GL, Price BH, Mesulam MM (1996) Right sided hemispatial neglect and bilateral cerebral lesions. J Neurol Neurosurg Psychiatry 60(3):342–344
Acknowledgements
We are thankful to Dr B. Batrancourt for managing the Centre for Cognitive Anatomy database project. We thank the Naturalia & Biologia Foundation for providing travel grants for some of the co-authors.
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The work of Dr Bartolomeo is supported by Agence Nationale de la Recherche through ANR-16-CE37-0005 and ANR-10-IAIHU-06.
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All the authors contributed to the study conception and design. Material preparation and data collection were performed by MNT. Analyses were performed by MNT and RM. The first draft of the manuscript was written by MNT, and all the authors commented on previous versions of the manuscript. All the authors read and approved the final manuscript.
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Toba, M.N., Migliaccio, R., Potet, A. et al. Right-side spatial neglect and white matter disconnection after left-hemisphere strokes. Brain Struct Funct 227, 2991–3000 (2022). https://doi.org/10.1007/s00429-022-02541-7
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DOI: https://doi.org/10.1007/s00429-022-02541-7