Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

A neuroanatomical model of space-based and object-centered processing in spatial neglect

  • 644 Accesses

  • 8 Citations

Abstract

Visual attention can be deployed in space-based or object-centered reference frames. Right-hemisphere damage may lead to distinct deficits of space- or object-based processing, and such dissociations are thought to underlie the heterogeneous nature of spatial neglect. Previous studies have suggested that object-centered processing deficits (such as in copying, reading or line bisection) result from damage to retro-rolandic regions while impaired spatial exploration reflects damage to more anterior regions. However, this evidence is based on small samples and heterogeneous tasks. Here, we tested a theoretical model of neglect that takes in account the space- and object-based processing and relates them to neuroanatomical predictors. One hundred and one right-hemisphere-damaged patients were examined with classic neuropsychological tests and structural brain imaging. Relations between neglect measures and damage to the temporal–parietal junction, intraparietal cortex, insula and middle frontal gyrus were examined with two structural equation models by assuming that object-centered processing (involved in line bisection and single-word reading) and space-based processing (involved in cancelation tasks) either represented a unique latent variable or two distinct variables. Of these two models the latter had better explanatory power. Damage to the intraparietal sulcus was a significant predictor of object-centered, but not space-based processing, while damage to the temporal–parietal junction predicted space-based, but not object-centered processing. Space-based processing and object-centered processing were strongly intercorrelated, indicating that they rely on similar, albeit partly dissociated processes. These findings indicate that object-centered and space-based deficits in neglect are partly independent and result from superior parietal and inferior parietal damage, respectively.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Asplund CL, Todd JJ, Snyder AP, Marois R (2010) A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention. Nat Neurosci 13:507–512

  2. Azouvi P et al (2002) Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. J Neurol Neurosurg Psychiatry 73:160–166

  3. Behrmann M, Tipper SP (1999) Attention accesses multiple reference frames: evidence from visual neglect. J Exp Psychol Hum Percept Perf 25:83–101

  4. Binder J, Marshall R, Lazar R, Benhamin J, Mohr JP (1992) Distinct syndromes of hemineglect. Arch Neurol 49:1187–1194

  5. Bisley JW, Goldberg ME (2010) Attention, intention, and priority in the parietal lobe. Ann Rev Neurosci 33:1–21

  6. Browne MW, Cudeck R (1993) Alternative ways of assessing model fit. In: Bollen KA, Long JS (eds) Testing structural equation models. Sage, Beverly Hills, pp 136–162

  7. Chechlacz M, Rotshtein P, Bickerton WL, Hansen PC, Deb S, Humphreys GW (2010) Separating neural correlates of allocentric and egocentric neglect: distinct cortical sites and common white matter disconnections. Cogn Neuropsychol 27:277–303

  8. Chechlacz M, Rotshtein P, Humphreys GW (2012) Neuroanatomical dissections of unilateral visual neglect symptoms: ALE meta-analysis of lesion-symptom mapping. Front Human Neurosci 6:230

  9. Committeri G et al (2007) Neural bases of personal and extrapersonal neglect in humans. Brain 130:431–441

  10. Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1990) Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248:1556–1559

  11. Doricchi F, Tomaiuolo F (2003) The anatomy of neglect without hemianopia: a key role for parietal-frontal disconnection? NeuroReport 14:2239–2243

  12. Driver J, Mattingley JB (1998) Parietal neglect and visual awareness. Nat Neurosci 1:17–22

  13. Driver J, Baylis GC, Goodrich SJ, Rafal RD (1994) Axis-based neglect of visual shapes. Neuropsychologia 32:1353–1365

  14. Duncan J (1984) Selective attention and the organization of visual information. J Exp Psychol Gen 113:501–517

  15. Egly R, Driver J, Rafal RD (1994) Shifting visual attention between objects and locations: evidence from normal and parietal lesion subjects. J Exp Psychol Gen 123:161–177

  16. Egner T, Monti JM, Trittschuh EH, Wieneke CA, Hirsch J, Mesulam MM (2008) Neural integration of top-down spatial and feature-based information in visual search. J Neurosci 28:6141–6151

  17. Ferber S, Karnath HO (2001) How to assess spatial neglect - line bisection or cancellation tasks? J Clin Exp Neropsychol 23:599–607

  18. Fink GR, Dolan RJ, Halligan PW, Marshall JC, Frith CD (1997) Space-based and object-based visual attention: shared and specific neural domains. Brain 120:2013–2028

  19. Friedman-Hill SR, Robertson LC, Treisman A (1995) Parietal contributions to visual feature binding: evidence from a patient with bilateral lesions. Science 269:853–855

  20. 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

  21. Gilchrist ID, Humphreys GW, Riddoch MJ (1996) Grouping and extinction: evidence for low-level modulation of visual selection. Cogn Neuropsychol 13:1223–1249

  22. Gillebert CR, Mantini D, Thijs V, Sunaert S, Dupont P, Vandenberghe R (2011) Lesion evidence for the critical role of the intraparietal sulcus in spatial attention. Brain 134:1694–1709

  23. Golay L, Schnider A, Ptak R (2008) Cortical and subcortical anatomy of chronic spatial neglect following vascular damage. Behav Brain Funct 4:43

  24. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

  25. Grimsen C, Hildebrandt H, Fahle M (2008) Dissociation of egocentric and allocentric coding of space in visual search after right middle cerebral artery stroke. Neuropsychologia 46:902–914

  26. Grosbras M-H, Laird AR, Paus T (2005) Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum Brain Mapp 25:140–154

  27. Halligan PW, Fink GR, Marshall JC, Vallar G (2003) Spatial cognition: evidence from visual neglect. Trends Cogn Sci 7:125–133

  28. He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M (2007) Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53:905–918

  29. Hillis AE (2006) Neurobiology of unilateral spatial neglect. Neuroscientist 12:153–163

  30. Himmelbach M, Erb M, Karnath H-O (2006) Exploring the visual world: the neural substrate of spatial orienting. NeuroImage 32:1747–1759

  31. Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods 6:53–60

  32. Hox JJ, Bechger TM (1998) An introduction to structural equation modeling. Fam Sci Rev 11:354–373

  33. Humphreys GW (1998) Neural representation of objects in space: a dual coding account. Phil Trans R Soc Lond B 353:1341–1351

  34. Husain M, Kennard C (1997) Distractor-dependent frontal neglect. Neuropsychologia 35:829–841

  35. Jerde TA, Merriam EP, Riggall AC, Hedges JH, Curtis CE (2012) Prioritized maps of space in human frontoparietal cortex. J Neurosci 32:17382–17390

  36. Karnath H-O, Rorden C (2012) The anatomy of spatial neglect. Neuropsychologia 50:1010–1017

  37. Karnath HO, Niemeier M, Dichgans J (1998) Space exploration in neglect. Brain 121:2357–2367

  38. 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

  39. Karnath H-O, Mandler A, Clavagnier S (2011) Object-based neglect varies with egocentric position. J Cogn Neurosci 23:2983–2993

  40. Lee BH et al (2009) Neglect dyslexia: frequency, association with other hemispatial neglects, and lesion localization. Neuropsychologia 47:704–710

  41. Leibovitch FS, Black SE, Caldwell CB, McIntosh AR, Ehrlich LE, Szalai JP (1999) Brain SPECT imaging and left hemispatial neglect covaried using partial least squares: the Sunnybrook Stroke Study. Hum Brain Mapp 7:244–253

  42. Losier BJW, Klein RM (2001) A review of the evidence for a disengage deficit following parietal lobe damage. Neurosci Biobehav Rev 25:1–13

  43. Manes F, Paradiso S, Springer JA, Lamberty G, Robinson RG (1999) Neglect after right insular cortex infarction. Stroke 30:946–948

  44. Marr D (1982) Vision. Freeman and Co., San Francisco

  45. McDonald RP, Ho MH (2002) Principles and practice in reporting structural equation analyses. Psychol Methods 7:64–82

  46. Medina J et al (2009) Neural substrates of visuospatial processing in distinct reference frames: evidence from unilateral spatial neglect. J Cogn Neurosci 21:2073–2084. doi:10.1162/jocn.2008.21160

  47. Molenberghs P, Sale MV, Mattingley JB (2012) Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation. Front Human Neurosci 6:78

  48. Mort DJ, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, Husain M (2003) The anatomy of visual neglect. Brain 126:1986–1997

  49. Mozer MC (2002) Frames of reference in unilateral neglect and visual perception: a computational perspective. Psychol Rev 109:156–185

  50. O’Craven KM, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Nature 401:584–587

  51. Ota H, Fujii T, Suzuki K, Fukatsu R, Yamadori A (2001) Dissociation of body-centered and stimulus-centered representations in unilateral neglect. Neurology 57:2064–2069

  52. Pedrazzini E, Fellrath J, Thézé R, Ptak R (2016) Electrophysiological correlates of visual binding errors after bilateral parietal damage. Neuroscience 337:98–106

  53. Ptak R, Fellrath J (2013) Spatial neglect and the neural coding of attentional priority. Neurosci Biobehav Rev 37:705–722

  54. Ptak R, Schnider A (2011) The attention network of the human brain: relating structural damage associated with spatial neglect to functional imaging correlates of spatial attention. Neuropsychologia 49:3063–3070

  55. Ptak R, Schnider A, Golay L, Müri R (2007) A non-spatial bias favouring fixated stimuli revealed in patients with spatial neglect. Brain 130:3211–3222

  56. Ptak R, Di Pietro M, Schnider A (2012) The neural correlates of object-centered processing in reading: a lesion study of neglect dyslexia. Neuropsychologia 50:1142–1150

  57. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  58. Rengachary J, He BJ, Shulman GL, Corbetta M (2011) A behavioral analysis of spatial neglect and its recovery after stroke. Front Human Neurosci 5:29

  59. Robertson LC (2004) Space, objects, minds, and brains. Psychology Press, New York and Hove

  60. Ronchi R, Algeri L, Chiapella L, Spada S, Vallar G (2012) Spatial neglect and perseveration in visuomotor exploration. Neuropsychology 26:588–603

  61. Rorden C, Fruhmann Berger M, Karnath H-O (2006) Disturbed line bisection is associated with posterior brain lesions. Brain Res 1080:17–25

  62. Rorden C, Karnath H-O, Bonilha L (2007) Improving lesion-symptom mapping. J Cogn Neurosci 19:1081–1088

  63. Rorden C, Bonilha L, Fridriksson J et al (2012) Age-specific CT and MRI templates for spatial normalization. Neuroimage 61:957–965

  64. Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Sotfware 48:1–36

  65. Serences JT, Schwarzbach J, Courtney SM, Golay X, Yantis S (2004) Control of object-based attention in human cortex. Cereb Cortex 14:1346–1357

  66. Shafritz KM, Gore JC, Marois R (2002) The role of the parietal cortex in visual feature binding. Proc Natl Acad Sci USA 99:10917–10922

  67. Singh-Curry V, Husain M (2009) The functional role of the inferior parietal lobe in the dorsal and ventral stream dichotomy. Neuropsychologia 47:1434–1448

  68. Treue S (2003) Visual attention: the where, what, how and why of saliency. Curr Opin Neurobiol 13:428–432

  69. Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, pp 549–586

  70. Urbanski M et al (2011) DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res 208:491–505

  71. 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

  72. Vandenberghe R, Molenbergs P, Gillebert CR (2012) Spatial attention deficits in humans: the critical role of superior compared to inferior parietal lesions. Neuropsychologia 50:1092–1103

  73. Verdon V, Schwartz S, Lovblad KO, Hauert CA, Vuilleumier P (2010) Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain 133:880–894

  74. Ward R, Goodrich S, Driver J (1994) Grouping reduces visual extinction: neuropsychological evidence for weight-linkage in visual selection. Visual Cognition 1:101–129

  75. Yantis S, Serences JT (2003) Cortical mechanisms of space-based and object-based attentional control. Curr Opin Neurobiol 13:187–193

  76. Zacks JM (2008) Neuroimaging studies of mental rotation: a meta-analysis and review. J Cogn Neurosci 20:1–19

Download references

Acknowledgements

Study supported by the Swiss National Science Foundation (Grant 320030-152689) and the Novartis Foundation for medical-biological Research (Grant 16C183).

Author information

Correspondence to Elena Pedrazzini or Radek Ptak.

Ethics declarations

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pedrazzini, E., Schnider, A. & Ptak, R. A neuroanatomical model of space-based and object-centered processing in spatial neglect. Brain Struct Funct 222, 3605–3613 (2017). https://doi.org/10.1007/s00429-017-1420-4

Download citation

Keywords

  • Spatial neglect
  • Visual attention
  • Parietal lobe
  • Attention network
  • Frontal lobe