Advertisement

Experimental Brain Research

, 200:109 | Cite as

Memory-guided saccade processing in visual form agnosia (patient DF)

  • Stéphanie Rossit
  • Larissa Szymanek
  • Stephen H. Butler
  • Monika HarveyEmail author
Research Article

Abstract

According to Milner and Goodale’s model (The visual brain in action, Oxford University Press, Oxford, 2006) areas in the ventral visual stream mediate visual perception and off-line actions, whilst regions in the dorsal visual stream mediate the on-line visual control of action. Strong evidence for this model comes from a patient (DF), who suffers from visual form agnosia after bilateral damage to the ventro-lateral occipital region, sparing V1. It has been reported that she is normal in immediate reaching and grasping, yet severely impaired when asked to perform delayed actions. Here we investigated whether this dissociation would extend to saccade execution. Neurophysiological studies and TMS work in humans have shown that the posterior parietal cortex (PPC), on the right in particular (supposedly spared in DF), is involved in the control of memory-guided saccades. Surprisingly though, we found that, just as reported for reaching and grasping, DF’s saccadic accuracy was much reduced in the memory compared to the stimulus-guided condition. These data support the idea of a tight coupling of eye and hand movements and further suggest that dorsal stream structures may not be sufficient to drive memory-guided saccadic performance.

Keywords

Memory-guided saccades Delay Eye movements Visual form agnosia Patient DF Dorsal and ventral stream Perception Action 

Notes

Acknowledgments

We would like to thank all the participants, DF in particular, for their time and patience and the reviewers of their most constructive comments on an earlier version of this manuscript. SR was funded by a Portuguese Foundation for Science and Technology grant (number SFRH/BD/23230/2005) and LS is funded by a Glasgow FIMS faculty scholarship.

References

  1. Barash S, Bracewell RM, Fogassi L, Gnadt JW, Andersen RA (1991) Saccade-related activity in the lateral intraparietal area: II. Spatial properties. J Neurophysiol 66:1109–1124PubMedGoogle Scholar
  2. Butler SH, Gilchrist ID, Ludwig JCH, Muir K, Harvey M (2006) Impairments of oculomotor control in a patient with a right temporo-parietal lesion. Cogn Neuropsychol 23:990–999CrossRefGoogle Scholar
  3. Butler SH, Rossit S, Gilchrist ID, Ludwig CJH, Olk B, Muir K, Reeves I, Harvey M (2009) Non-lateralised deficits in anti-saccade performance in patients with hemispatial neglect. Neuropsychologia 47:2488–2495CrossRefPubMedGoogle Scholar
  4. Cohen-Rice N, Cross ES, Tunik E, Grafton ST, Culham JC (2009) Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: a TMS approach. Neuropsychologia 47:1553–1562CrossRefGoogle Scholar
  5. Colby CL, Duhamel JR, Goldberg ME (1996) Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 76:2841–2852PubMedGoogle Scholar
  6. Connolly JD, Goodale MA, Menon RS, Munoz DP (2002) Human fMRI evidence for the neural correlates of preparatory set. Nat Neurosci 5:1345–1352CrossRefPubMedGoogle Scholar
  7. Crawford JR, Howell DC (1998) Comparing an individual’s test score against norms derived from small samples. Clin Neuropsychol 12:482–486Google Scholar
  8. Curtis CE, D’Esposito M (2006) Selection and maintenance of saccade goals in the human frontal eye fields. J Neurophysiol 95:3923–3927CrossRefPubMedGoogle Scholar
  9. Dijkerman HC, Milner AD, Carey DP (1997) Impaired delayed and anti-saccades in a visual form agnosic. Exp Brain Res 117(suppl):S66Google Scholar
  10. Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885–899CrossRefPubMedGoogle Scholar
  11. Glimcher PW (2003) The neurobiology of visual-saccadic decision making. Annu Rev Neurosci 26:133–179CrossRefPubMedGoogle Scholar
  12. Gnadt JW, Anderson RA (1988) Memory related motor planning activity in posterior parietal cortex of macaque. Exp Brain Res 70:216–220PubMedGoogle Scholar
  13. Goldberg ME, Bisley J, Powell KD, Gottlieb J, Kusunoki M (2002) The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention. Ann NY Acad Sci 956:205–215CrossRefPubMedGoogle Scholar
  14. Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends in Neurosci 15:20–25CrossRefGoogle Scholar
  15. Goodale MA, Jakobson LS, Keillor JM (1994) Differences in the visual control of pantomimed and natural grasping movements. Neuropsychologia 32:1159–1178CrossRefPubMedGoogle Scholar
  16. Grefkes C, Fink GR (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17CrossRefPubMedGoogle Scholar
  17. Hagler DJ Jr, Riecke L, Sereno MI (2007) Parietal and superior frontal visuospatial maps activated by pointing and saccades. Neuroimage 35:1562–1577CrossRefPubMedGoogle Scholar
  18. Himmelbach M, Nau M, Zündorf I, Erb M, Perenin MT, Karnath HO (2009) Brain activation during immediate and delayed reaching in optic ataxia. Neuropsychologia 47:1508–1517CrossRefPubMedGoogle Scholar
  19. Humphrey K, Goodale MA, Jakobson LS, Servos P (1994) The role of surface information in object recognition: studies of a visual form agnostic and normal subjects. Perception 23:1457–1481CrossRefPubMedGoogle Scholar
  20. James WT, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesion impair object recognition but not object-directed grasping: an fMRI study. Brain 126:2463–2475CrossRefPubMedGoogle Scholar
  21. Karnath HO, Ferber S, Himmelbach M (2001) Spatial awareness is a function of the temporal noth the posterior parietal lobe. Nature 411:950–953CrossRefPubMedGoogle Scholar
  22. Karnath HO, Berger MF, Kuker W, Rorden C (2004) The anatomy of spatial neglect based on voxelvise statistical analysis: a study of 140 patients. Cereb Cortex 14:1164–1172CrossRefPubMedGoogle Scholar
  23. Levy I, Schluppeck D, Heeger DJ, Glimcher PW (2007) Specificity of human cortical areas for reaches and saccades. J Neurosci 27:4687–4696CrossRefPubMedGoogle Scholar
  24. Milner AD (1995) Cerebral correlates of visual awareness. Neurospychologia 33:1117–1130CrossRefGoogle Scholar
  25. Milner AD (1997) Neglect, extinction and the cortical streams of visual processing. In: Thier P, Karnath H-O (eds) Parietal lobe contributions to orientation in 3D space. Springer, Heidelberg, pp 3–22Google Scholar
  26. Milner AD (1998a) Streams and consciousness: visual awareness and the brain. Trends Cogn Sci 2:25–30CrossRefGoogle Scholar
  27. Milner AD (1998b) Neuropsychological studies of perception and visuomotor control. Philos Trans R Soc Lond B Biol Sci 353:1375–1384CrossRefPubMedGoogle Scholar
  28. Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, OxfordGoogle Scholar
  29. Milner AD, Goodale MA (2006) The visual brain in action, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  30. Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46:774–785CrossRefPubMedGoogle Scholar
  31. Milner AD, Perrett DI, Johnston RS, Benson PJ, Jordan TR, Heeley DW, Bettucci D, Mortana F, Mutani R, Terazzi E, Davidson DLW (1991) Perception and action in ‘visual form agnosia’. Brain 114:405–428CrossRefPubMedGoogle Scholar
  32. Milner AD, Dijkerman HC, Carey DP (1999a) Visuospatial processing in a pure case of visual from agnosia. In: Burgess N, Jeffrey KJ, O’Keefe J (eds) The hippocampal and parietal functions of spatial cognition. Oxford University Press, Oxford, pp 443–466Google Scholar
  33. Milner AD, Paulignan Y, Dijkerman HC, Michel F, Jeannerod M (1999b) A paradoxical improvement of misreaching in optic ataxia: new evidence for two separate neural systems for visual localization. Proc Biol Sci-B 266:2225–2229CrossRefGoogle Scholar
  34. Milner AD, Dijkerman HC, Pisella L, McIntosh RD, Tilikete C, Vigetto A, Rossetti Y (2001) Grasping the past: delay can improve visuomotor performance. Curr Biol 11:1896–1901CrossRefPubMedGoogle Scholar
  35. Mort JD, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, Husain M (2003) The anatomy of visual neglect. Brain 126:1986–1997CrossRefPubMedGoogle Scholar
  36. Mueri RM, Vermerschm AI, Rivaud S, Gaymard B, Pierrot-Deseilligny C (1996) Effects of single pulse transcranial magnetic stimulation over the prefrontal and posterior parietal cortices during memory-guided saccades in humans. J Neurophysiol 76:2102–2106Google Scholar
  37. Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218–228CrossRefPubMedGoogle Scholar
  38. Nyffeler T, Egli A, Pflugshaupt T, von Wartburg R, Wurtz P, Mosimann U, Hess CW, Mueri RM (2005) The role of the human posterior parietal cortex in memory-guided saccade execution: a double-pulse transcranial magnetic stimulation study. Eur J Neurosci 22:535–538CrossRefPubMedGoogle Scholar
  39. Rossit S, Malhotra P, Muir K, Duncan G, Reeves I, Birschel P, Harvey M (2009a) The neural basis of visuomotor deficits in hemispatial neglect. Neuropsychologia 47:2149–2153CrossRefPubMedGoogle Scholar
  40. Rossit S, Muir K, Reeves I, Duncan G, Birschel P, Harvey M (2009b) Immediate and delayed reaching in hemispatial neglect. Neuropsychologia 47:1563–1572CrossRefPubMedGoogle Scholar
  41. Schluppeck D, Curtis CE, Glimcher PW, Heeger DJ (2006a) Sustained activity in topographic areas of human posterior parietal cortex during memory-guided saccades. J Neurosci 26:5098–5108CrossRefPubMedGoogle Scholar
  42. Schluppeck D, Glimcher P, Heeger DJ (2006b) Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol 94:1372–1384CrossRefGoogle Scholar
  43. Snyder LH, Batista AP, Andersen RA (2000) Saccade-related activity in the parietal reach region. J Neurophysiol 83:1099–1102PubMedGoogle Scholar
  44. Westwood DA, Goodale MA (2003) Perceptual illusion and the real-time control of action. Spat Vis 16:243–254CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Stéphanie Rossit
    • 1
  • Larissa Szymanek
    • 2
  • Stephen H. Butler
    • 3
  • Monika Harvey
    • 2
    Email author
  1. 1.Department of PsychologyUniversity of Western OntarioLondonCanada
  2. 2.Department of PsychologyUniversity of GlasgowGlasgowScotland, UK
  3. 3.Department of PsychologyUniversity of StrathclydeGlasgowUK

Personalised recommendations