Model approach to neurological variants of visuo-spatial neglect

Abstract

Neglect is a neurological disorder of spatial attention with reduced awareness of visual stimuli in the hemifield contralateral to an acute temporo-parietal lesion mainly of the right hemisphere. There is a close association of multisensory orientation centers (MSO) and vestibular tonus imbalance. A lesion of the dominant right MSO causes a left-sided neglect due to a lack of ipsilateral activation of the visual cortex, which is further enhanced by increasing inhibition from the contralateral visual cortex. The nondominant MSO in the left hemisphere might be involved in the manifestation of the less frequent and more transient right-sided neglect and in the plastic mechanisms of gradual recovery from left-sided neglect or extinction. There is evidence that a vestibular tonus inbalance due to peripheral or central vestibular pathway lesions may also induce a neglect. In a first model approach using an attractor network and assuming that there is only one MSO in the right hemisphere, it is possible to simulate attentional shifts into a visual hemifield and to induce a neglect. The neural network model consists of four layers of neurons: retina, MSO, visual cortex V1, and superior colliculus. The superior colliculus layer is modeled as a recurrent attractor network with one inhibitory interneuron and synaptic weights chosen to implement a winner-take-all network that centers the hill of activity on the strongest input. We are well aware of the simplifications used in the conceptual drawings and the computational model, but nevertheless hope that they will serve as an inspiration for further modeling and clinical studies.

This is a preview of subscription content, access via your institution.

References

  1. Baier B, Karnath H-O, Thömke F et al (2010) Is there a link between spatial neglect and vestibular function at the cerebellar level?. J Neurol 257: 1579–1581

    PubMed  Article  Google Scholar 

  2. Becker E, Karnath H-O (2007) Incidence of visual extinction after left versus right hemisphere stroke. Stroke 38: 3172–3174

    PubMed  Article  Google Scholar 

  3. Bense S, Bartenstein P, Lochmann M et al (2004) Metabolic changes in vestibular and visual cortices in acute vestibular neuritis. Ann Neurol 56: 624–630

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  5. Brandt T (1999) Vertigo, its multisensory syndromes, 2nd ed. Springer, London

    Google Scholar 

  6. Brandt T, Dieterich M (1994) Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol 36: 337–347

    CAS  PubMed  Article  Google Scholar 

  7. Brandt T, Dieterich M, Danek A (1994) Vestibular cortex lesions affect the perception of verticality. Ann Neurol 35: 528–534

    Article  Google Scholar 

  8. Brandt T, Bucher SF, Seelos KC et al (1998) Bilateral functional MRI activation of the basal ganglia and middle temporal/medial superior temporal motion sensitive areas: Optokinetic stimulation in homonymous hemianopia. Arch Neurol 55: 1126–1131

    CAS  PubMed  Article  Google Scholar 

  9. Brandt T, Stephan T, Bense S et al (2000) Hemifield visual motion stimulation: an example of interhemispheric crosstalk. Neuroreport 11: 2803–2809

    CAS  PubMed  Article  Google Scholar 

  10. Brandt T, Glasauer S, Stephan T et al (2002) Visual-vestibular and visuovisual cortical interaction: new insights from fMRI and PET. Ann N Y Acad Sci 956: 230–241

    PubMed  Article  Google Scholar 

  11. Brandt T, Marx E, Stephan T et al (2003) Inhibitory interhemispheric visuovisual interaction in motion perception. Ann N Y Acad Sci 1004: 283–288

    PubMed  Article  Google Scholar 

  12. Brandt T, Glasauer S, Strupp M, Dieterich M (2009) Spatial neglect: hypothetical mechanisms of disturbed interhemispheric crosstalk for orientation. Ann N Y Acad Sci 1164: 216–221

    PubMed  Article  Google Scholar 

  13. Cappa S, Sterzi R, Vallar G et al (1987) Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia 25: 775–782

    CAS  PubMed  Article  Google Scholar 

  14. Cazzoli D, Schumacher R, Baas U et al (2012) Bilateral neglect after bihemispheric strokes. Cortex 48: 504–508

    PubMed  Article  Google Scholar 

  15. Choi K-D, Jo M-K, Kim M-J et al (2012) Vestibular hemispatial neglect: Patterns and possible mechanisms. (Submitted)

  16. Corbetta M, Shulman GL (2011) Spatial neglect and attention networks. Annu Rev Neurosci 34: 569–599

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  17. De Witte L, Verhoeven J, Engelborghs S et al (2008) Crossed aphasia and visuo-spatial neglect following a right thalamic stroke: a case study and review of the literature. Behav Neurol 19: 177–194

    PubMed  Article  Google Scholar 

  18. Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131: 2538–2552

    PubMed  Article  Google Scholar 

  19. Dieterich M, Bense S, Lutz S et al (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13: 994–1007

    CAS  PubMed  Article  Google Scholar 

  20. Dieterich M, Bartenstein P, Spiegel S et al (2005a) Thalamic infarctions cause side-specific suppression of vestibular cortex activations. Brain 128: 2052–2067

    CAS  PubMed  Article  Google Scholar 

  21. Dieterich M, Bense S, Stephan T et al (2005b) Medial vestibular nucleus lesions in Wallenberg’s syndrome cause decreased activity of the contralateral vestibular cortex. Ann N Y Acad Sci 1039: 368–383

    PubMed  Article  Google Scholar 

  22. Dieterich M, Bense S, Spiegel S et al (2005c) Thalamic infarctions cause side-specific suppression of vestibular cortex activations. Brain 128: 2052–2067

    CAS  PubMed  Article  Google Scholar 

  23. Dieterich M, Bense S, Buchholz H-G et al (2012) On the differential effects of acute right vs. left-sided vestibular failure on brain metabolism. (Submitted)

  24. Dronkers NF, Knight RT (1989) Right-sided neglect in a left-hander: evidence for reversed hemispheric specialization of attention capacity. Neuropsychology 27: 729–735

    CAS  Article  Google Scholar 

  25. Goodridge JP, Touretzky DS (2000) Modeling attractor deformation in the rodent head-direction system. J Neurophysiol 83: 3402–3410

    CAS  PubMed  Google Scholar 

  26. Halligan PW, Marshall J (1998) Visuospatial neglect: the ultimate deconstruction. Brain Cogn 37: 419–438

    CAS  PubMed  Article  Google Scholar 

  27. Heinke D, Deco G, Zihl J, Humphreys GW (2002) A computational neuroscience account of visual neglect. Neurocomputing 44(1–4): 811–816

    Article  Google Scholar 

  28. Hildebrandt H, Spang K, Ebke M (2002) Visuospatial hemi-inattention following cerebellar/brain stem bleeding. Neurocase 8: 323–339

    CAS  PubMed  Article  Google Scholar 

  29. Hilgetag CC (2000) Spatial neglect and paradoxical lesion effects in the cat—a model based on midbrain connectivity. Neurocomputing 32–33: 793–799

    Article  Google Scholar 

  30. Hilgetag C, Théoret H, Pascual-Leone A (2001) Enhanced visual spatial attention ipsilateral to rTMS-induced “virtual lesions” of human parietal cortex. Nat Neurosci 9: 953–957

    Article  Google Scholar 

  31. Humphreys GW, Riddoch MJ (1994) Attention to within-object and between object spatial representations: multiple sites for visual selection. Cogn Neuropsychol 11: 207–241

    Article  Google Scholar 

  32. Husain M, Kennard C (1996) Visual neglect associated with frontal lobe infarction. J Neurol 243: 652–657

    CAS  PubMed  Article  Google Scholar 

  33. Karnath H-O (1999) Subjective body orientation in neglect and the interactive contribution of neck muscle proprioception and vestibular stimulation. Brain 117: 1001–1012

    Article  Google Scholar 

  34. Karnath H-O, Dieterich M (2006) Spatial neglect—a vestibular disorder?. Brain 129: 293–305

    PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  Google Scholar 

  36. Karnath H-O, Fruhmann-Berger M, Küker W, Rordon C (2004) The anatomy of cortical neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14: 1164–1172

    PubMed  Article  Google Scholar 

  37. Kerkhoff G, Schenk T (2012) Rehabilitation of neglect: an update. Neuropsychologia 50: 1072–1079

    PubMed  Article  Google Scholar 

  38. Kim EJ, Choi KD, Han MK et al (2008) Hemispatial neglect in cerebellar stroke. J Neurol Sci 275: 133–138

    CAS  PubMed  Article  Google Scholar 

  39. Lomber SG, Payne BR (1996) Removal of the two halves restores the whole: reversal of visual hemineglect during bilateral cortical or collicular inactivation in the cat. Vis Neurosci 13: 1143–1156

    CAS  PubMed  Article  Google Scholar 

  40. Lomber SG, Payne BR (2001) Task-specific reversal of visual hemineglect during reversible deactivation of posterior parietal cortex: a comparison with deactivation of the superior colliculus. Vis Neurosci 18: 487–499

    CAS  PubMed  Article  Google Scholar 

  41. Maeshima S, Terada T, Nakai K et al (1995) Unilateral spatial neglect due to a haemorrhagic contusion in the right frontal lobe. J Neurol 242: 613–617

    CAS  PubMed  Article  Google Scholar 

  42. McGlinchey-Berroth R, Bullis DP, Milberg WP et al (1996) Assessment of neglect reveals dissociable behavioural but not neuroanatomical subtypes. J Intern Neuropsychol 2: 441–451

    CAS  Article  Google Scholar 

  43. Monaghan P, Shillcock R (2004) Hemispheric asymmetries in cognitive modeling: connectionist modeling of unilateral visual neglect. Psychol Rev 111: 283–308

    PubMed  Article  Google Scholar 

  44. Oliveri M (2011) Brain stimulation procedures for treatment of contralesional spatial neglect. Restor Neurol Neurosci 29: 421–425

    PubMed  Google Scholar 

  45. Payne BR, Rushmore R-J (2004) Functional circuitry underlying natural and interventional cancellation of visual neglect. Exp Brain Res 154: 127–153

    PubMed  Article  Google Scholar 

  46. Pisella L, Mattingley JB (2004) The contribution of spatial remapping impairments to unilateral visual neglect. Neurosci Behav Rev 28: 181–200

    Article  Google Scholar 

  47. 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

    PubMed  Article  Google Scholar 

  48. Ptak R, Schnider A, Müri R (2010) Bilateral impairment of concurrent saccade programming in hemispatial neglect. Neuropsychologia 48: 880–886

    PubMed  Article  Google Scholar 

  49. Rushmore RJ, Valero-Cabre A, Lomber SG et al (2006) Functional circuitry underlying visual neglect. Brain 129: 1803–1821

    PubMed  Article  Google Scholar 

  50. Silveri MC, Misciagna S, Terrezza G (2001) Right side neglect in right cerebellar lesion. J Neurol Neurosurg Psychiatry 71: 114–117

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  51. Vallar G, Perani D (1986) The anatomy of unilateral neglect after right hemisphere stroke lesions: a clinical CT correlation study in man. Neuropsychologia 24: 609–622

    CAS  PubMed  Article  Google Scholar 

  52. Vallar G, Bottini G, Rusconi ML et al (1993) Exploring somatosensory hemineglect by vestibular stimulation. Brain 116: 71–86

    PubMed  Article  Google Scholar 

  53. Vanderploeg RD (1986) Left-handedness and variant patterns of cerebral organization: a case study. Arch Clin Neuropsychol 1: 357–369

    CAS  PubMed  Article  Google Scholar 

  54. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12: 1–24

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  55. Zu Eulenburg P, Caspers S, Roski C et al (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60: 162–169

    CAS  PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Thomas Brandt.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Brandt, T., Dieterich, M., Strupp, M. et al. Model approach to neurological variants of visuo-spatial neglect. Biol Cybern 106, 681–690 (2012). https://doi.org/10.1007/s00422-012-0517-3

Download citation

Keywords

  • Visuo-spatial neglect
  • Modeling
  • Visual cortex
  • Vestibular cortex