Advertisement

Brain Structure and Function

, Volume 222, Issue 2, pp 1093–1107 | Cite as

Dorsal and ventral stream contributions to form-from-motion perception in a patient with form-from motion deficit: a case report

  • Manuel R. Mercier
  • Sophie Schwartz
  • Laurent Spinelli
  • Christoph M. Michel
  • Olaf Blanke
Short Communication

Abstract

The main model of visual processing in primates proposes an anatomo-functional distinction between the dorsal stream, specialized in spatio-temporal information, and the ventral stream, processing essentially form information. However, these two pathways also communicate to share much visual information. These dorso-ventral interactions have been studied using form-from-motion (FfM) stimuli, revealing that FfM perception first activates dorsal regions (e.g., MT+/V5), followed by successive activations of ventral regions (e.g., LOC). However, relatively little is known about the implications of focal brain damage of visual areas on these dorso-ventral interactions. In the present case report, we investigated the dynamics of dorsal and ventral activations related to FfM perception (using topographical ERP analysis and electrical source imaging) in a patient suffering from a deficit in FfM perception due to right extrastriate brain damage in the ventral stream. Despite the patient’s FfM impairment, both successful (observed for the highest level of FfM signal) and absent/failed FfM perception evoked the same temporal sequence of three processing states observed previously in healthy subjects. During the first period, brain source localization revealed cortical activations along the dorsal stream, currently associated with preserved elementary motion processing. During the latter two periods, the patterns of activity differed from normal subjects: activations were observed in the ventral stream (as reported for normal subjects), but also in the dorsal pathway, with the strongest and most sustained activity localized in the parieto-occipital regions. On the other hand, absent/failed FfM perception was characterized by weaker brain activity, restricted to the more lateral regions. This study shows that in the present case report, successful FfM perception, while following the same temporal sequence of processing steps as in normal subjects, evoked different patterns of brain activity. By revealing a brain circuit involving the most rostral part of the dorsal pathway, this study provides further support for neuro-imaging studies and brain lesion investigations that have suggested the existence of different brain circuits associated with different profiles of interaction between the dorsal and the ventral streams.

Keywords

Perceptual deficit Form-from-motion EEG Brain lesion 

Notes

Acknowledgments

The authors would like to express their gratitude to the patient for her time and her patience during the investigations. We also would like to thank Arnaud Saj for providing precious information regarding patient history and we are extremely grateful to Nihaad Paraouty, Grace Edwards and Douglas McLelland for English editing. This research was funded by the Swiss National Science Foundation (Grants 310000-114008 and 3200B0-104100) and the Swiss Center for Affective Sciences. The Cartool software (http://brainmapping.unige.ch/cartool) has been programmed by Denis Brunet, from the Functional Brain Mapping Laboratory, Geneva, Switzerland, and is supported by the Center for Biomedical Imaging (CIBM) of Geneva and Lausanne. This experiment was realized using Cogent Graphics developed by John Romaya at the LON at the Wellcome Department of Imaging Neuroscience.

References

  1. Andersen RA (1989) Visual and eye movement functions of the posterior parietal cortex. Annu Rev Neurosci 12:377–403. doi: 10.1146/annurev.ne.12.030189.002113 CrossRefPubMedGoogle Scholar
  2. Andersen RA, Bradley DC (1998) Perception of three-dimensional structure from motion. Trends Cogn Sci 2(6):222–228CrossRefPubMedGoogle Scholar
  3. Barton JJ, Sharpe JA, Raymond JE (1995) Retinotopic and directional defects in motion discrimination in humans with cerebral lesions. Ann Neurol 37(5):665–675. doi: 10.1002/ana.410370517 CrossRefPubMedGoogle Scholar
  4. Blanke O, Brooks A, Mercier M, Spinelli L, Adriani M, Lavanchy L, Safran AB, Landis T (2007) Distinct mechanisms of form-from-motion perception in human extrastriate cortex. Neuropsychologia 45(4):644–653CrossRefPubMedGoogle Scholar
  5. Born RT, Bradley DC (2005) Structure and function of visual area MT. Annu Rev Neurosci 28:157–189. doi: 10.1146/annurev.neuro.26.041002.131052 CrossRefPubMedGoogle Scholar
  6. Braddick OJ, O’Brien JM, Wattam-Bell J, Atkinson J, Turner R (2000) Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain. Curr Biol 10(12):731–734CrossRefPubMedGoogle Scholar
  7. Bradley DC, Chang GC, Andersen RA (1998) Encoding of three-dimensional structure-from-motion by primate area MT neurons. Nature 392(6677):714–717. doi: 10.1038/33688 CrossRefPubMedGoogle Scholar
  8. Brouwer GJ, van Ee R (2007) Visual cortex allows prediction of perceptual states during ambiguous structure-from-motion. J Neurosci 27(5):1015–1023. doi: 10.1523/JNEUROSCI.4593-06.2007 CrossRefPubMedGoogle Scholar
  9. Brunet D, Murray MM, Michel CM (2011) Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci 2011:813870. doi: 10.1155/2011/813870 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bullier J (2001) Integrated model of visual processing. Brain Res Brain Res Rev 36(2–3):96–107CrossRefPubMedGoogle Scholar
  11. Castelo-Branco M, Mendes M, Silva MF, Januario C, Machado E, Pinto A, Figueiredo P, Freire A (2006) Specific retinotopically based magnocellular impairment in a patient with medial visual dorsal stream damage. Neuropsychologia 44(2):238–253. doi: 10.1016/j.neuropsychologia.2005.05.005 CrossRefPubMedGoogle Scholar
  12. Cottereau BR, McKee SP, Norcia AM (2014) Dynamics and cortical distribution of neural responses to 2D and 3D motion in human. J Neurophysiol 111(3):533–543. doi: 10.1152/jn.00549.2013 CrossRefPubMedGoogle Scholar
  13. Cowey A, Vaina LM (2000) Blindness to form from motion despite intact static form perception and motion detection. Neuropsychologia 38(5):566–578CrossRefPubMedGoogle Scholar
  14. de Jong BM, Shipp S, Skidmore B, Frackowiak RS, Zeki S (1994) The cerebral activity related to the visual perception of forward motion in depth. Brain 117(Pt 5):1039–1054CrossRefPubMedGoogle Scholar
  15. Dodd JV, Krug K, Cumming BG, Parker AJ (2001) Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J Neurosci 21(13):4809–4821PubMedGoogle Scholar
  16. Dupont P, Orban GA, De Bruyn B, Verbruggen A, Mortelmans L (1994) Many areas in the human brain respond to visual motion. J Neurophysiol 72(3):1420–1424PubMedGoogle Scholar
  17. Dupont P, De Bruyn B, Vandenberghe R, Rosier AM, Michiels J, Marchal G, Mortelmans L, Orban GA (1997) The kinetic occipital region in human visual cortex. Cereb Cortex 7(3):283–292CrossRefPubMedGoogle Scholar
  18. Fattori P, Pitzalis S, Galletti C (2009) The cortical visual area V6 in macaque and human brains. J Physiol Paris 103(1–2):88–97. doi: 10.1016/j.jphysparis.2009.05.012 CrossRefPubMedGoogle Scholar
  19. Ferber S, Humphrey GK, Vilis T (2003) The lateral occipital complex subserves the perceptual persistence of motion-defined groupings. Cereb Cortex 13(7):716–721CrossRefPubMedGoogle Scholar
  20. Galletti C, Fattori P (2003) Neuronal mechanisms for detection of motion in the field of view. Neuropsychologia 41(13):1717–1727CrossRefPubMedGoogle Scholar
  21. Gilaie-Dotan S (2015) Which visual functions depend on intermediate visual regions? Insights from a case of developmental visual form agnosia. Neuropsychologia. doi: 10.1016/j.neuropsychologia.2015.07.023 PubMedGoogle Scholar
  22. Gilaie-Dotan S, Bentin S, Harel M, Rees G, Saygin AP (2011) Normal form from biological motion despite impaired ventral stream function. Neuropsychologia 49(5):1033–1043. doi: 10.1016/j.neuropsychologia.2011.01.009 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gilaie-Dotan S, Saygin AP, Lorenzi LJ, Egan R, Rees G, Behrmann M (2013) The role of human ventral visual cortex in motion perception. Brain 136(Pt 9):2784–2798. doi: 10.1093/brain/awt214 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Goebel R, Khorram-Sefat D, Muckli L, Hacker H, Singer W (1998) The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur J Neurosci 10(5):1563–1573CrossRefPubMedGoogle Scholar
  25. Gonzalez Andino SL, de Peralta Grave, Menendez R, Lantz CM, Blank O, Michel CM, Landis T (2001) Non-stationary distributed source approximation: an alternative to improve localization procedures. Hum Brain Mapp 14(2):81–95CrossRefPubMedGoogle Scholar
  26. Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25CrossRefPubMedGoogle Scholar
  27. Grave de Peralta Menendez R, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL (2004) Electrical neuroimaging based on biophysical constraints. Neuroimage 21(2):527–539CrossRefPubMedGoogle Scholar
  28. Grill-Spector K, Kushnir T, Edelman S, Itzchak Y, Malach R (1998) Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21(1):191–202CrossRefPubMedGoogle Scholar
  29. Grunewald A, Bradley DC, Andersen RA (2002) Neural correlates of structure-from-motion perception in macaque V1 and MT. J Neurosci 22(14):6195–6207PubMedGoogle Scholar
  30. Gulyas B, Heywood CA, Popplewell DA, Roland PE, Cowey A (1994) Visual form discrimination from color or motion cues: functional anatomy by positron emission tomography. Proc Natl Acad Sci USA 91(21):9965–9969CrossRefPubMedPubMedCentralGoogle Scholar
  31. Heinrich SP (2007) A primer on motion visual evoked potentials. Doc Ophthalmol 114(2):83–105CrossRefPubMedGoogle Scholar
  32. Jiang Y, Boehler CN, Nonnig N, Duzel E, Hopf JM, Heinze HJ, Schoenfeld MA (2008) Binding 3-D object perception in the human visual cortex. J Cogn Neurosci 20(4):553–562. doi: 10.1162/jocn.2008.20050 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kuba M, Kubova Z, Kremlacek J, Langrova J (2007) Motion-onset VEPs: characteristics, methods, and diagnostic use. Vision Res 47(2):189–202CrossRefPubMedGoogle Scholar
  34. Lehmann D, Ozaki H, Pal I (1987) EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. Electroencephalogr Clin Neurophysiol 67(3):271–288CrossRefPubMedGoogle Scholar
  35. Lopez C, Mercier MR, Halje P, Blanke O (2011) Spatiotemporal dynamics of visual vertical judgments: early and late brain mechanisms as revealed by high-density electrical neuroimaging. Neuroscience 181:134–149. doi: 10.1016/j.neuroscience.2011.02.009 CrossRefPubMedGoogle Scholar
  36. Losey F, Safran AB, Mermound C, Michel C, Landis T (1998) Visual perception of movement. A normative study. Klin Monbl Augenheilkd 212(5):379–381. doi: 10.1055/s-2008-1034911 CrossRefPubMedGoogle Scholar
  37. Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92(18):8135–8139CrossRefPubMedPubMedCentralGoogle Scholar
  38. Matheson HE, McMullen PA (2010) Neuropsychological dissociations between motion and form perception suggest functional organization in extrastriate cortical regions in the human brain. Brain Cogn 74(2):160–168. doi: 10.1016/j.bandc.2010.07.009 CrossRefPubMedGoogle Scholar
  39. Maunsell JH, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–401. doi: 10.1146/annurev.ne.10.030187.002051 CrossRefPubMedGoogle Scholar
  40. Mercier M, Schwartz S, Michel CM, Blanke O (2009) Motion direction tuning in human visual cortex. Eur J Neurosci 29(2):424–434. doi: 10.1111/j.1460-9568.2008.06583.x CrossRefPubMedGoogle Scholar
  41. Michel CM, Murray MM (2012) Towards the utilization of EEG as a brain imaging tool. Neuroimage 61(2):371–385. doi: 10.1016/j.neuroimage.2011.12.039 CrossRefPubMedGoogle Scholar
  42. Michel CM, Grave de Peralta R, Lantz G, Gonzalez Andino S, Spinelli L, Blanke O, Landis T, Seeck M (1999) Spatiotemporal EEG analysis and distributed source estimation in presurgical epilepsy evaluation. J Clin Neurophysiol 16(3):239–266CrossRefPubMedGoogle Scholar
  43. Michel CM, Thut G, Morand S, Khateb A, Pegna AJ, Grave de Peralta R, Gonzalez S, Seeck M, Landis T (2001) Electric source imaging of human brain functions. Brain Res Brain Res Rev 36(2–3):108–118CrossRefPubMedGoogle Scholar
  44. Mishkin M, Ungerleider LG (1982) Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav Brain Res 6(1):57–77CrossRefPubMedGoogle Scholar
  45. Murray SO, Olshausen BA, Woods DL (2003) Processing shape, motion and three-dimensional shape-from-motion in the human cortex. Cereb Cortex 13(5):508–516CrossRefPubMedGoogle Scholar
  46. Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20(4):249–264CrossRefPubMedGoogle Scholar
  47. Niedeggen M, Wist ER (1999) Characteristics of visual evoked potentials generated by motion coherence onset. Brain Res Cogn Brain Res 8(2):95–105CrossRefPubMedGoogle Scholar
  48. Orban GA, Sunaert S, Todd JT, Van Hecke P, Marchal G (1999) Human cortical regions involved in extracting depth from motion. Neuron 24(4):929–940CrossRefPubMedGoogle Scholar
  49. Paradis AL, Cornilleau-Peres V, Droulez J, Van De Moortele PF, Lobel E, Berthoz A, Le Bihan D, Poline JB (2000) Visual perception of motion and 3-D structure from motion: an fMRI study. Cereb Cortex 10(8):772–783CrossRefPubMedGoogle Scholar
  50. Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42(7):658–665CrossRefPubMedGoogle Scholar
  51. Peuskens H, Claeys KG, Todd JT, Norman JF, Van Hecke P, Orban GA (2004) Attention to 3-D shape, 3-D motion, and texture in 3-D structure from motion displays. J Cogn Neurosci 16(4):665–682. doi: 10.1162/089892904323057371 CrossRefPubMedGoogle Scholar
  52. Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI (2006) Wide-field retinotopy defines human cortical visual area v6. J Neurosci 26(30):7962–7973. doi: 10.1523/JNEUROSCI.0178-06.2006 CrossRefPubMedGoogle Scholar
  53. Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Patria F, Galletti C (2010) Human v6: the medial motion area. Cereb Cortex 20(2):411–424. doi: 10.1093/cercor/bhp112 CrossRefPubMedGoogle Scholar
  54. Pitzalis S, Sdoia S, Bultrini A, Committeri G, Di Russo F, Fattori P, Galletti C, Galati G (2013) Selectivity to translational egomotion in human brain motion areas. PLoS One 8(4):e60241. doi: 10.1371/journal.pone.0060241 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Plomp G, Mercier MR, Otto TU, Blanke O, Herzog MH (2009) Non-retinotopic feature integration decreases response-locked brain activity as revealed by electrical neuroimaging. Neuroimage 48(2):405–414. doi: 10.1016/j.neuroimage.2009.06.031 CrossRefPubMedGoogle Scholar
  56. Regan D, Giaschi D, Sharpe JA, Hong XH (1992) Visual processing of motion-defined form: selective failure in patients with parietotemporal lesions. J Neurosci 12(6):2198–2210PubMedGoogle Scholar
  57. Schenk T, Zihl J (1997) Visual motion perception after brain damage: II. Deficits in form-from-motion perception. Neuropsychologia 35(9):1299–1310CrossRefPubMedGoogle Scholar
  58. Schoenfeld MA, Woldorff M, Duzel E, Scheich H, Heinze HJ, Mangun GR (2003) Form-from-motion: MEG evidence for time course and processing sequence. J Cogn Neurosci 15(2):157–172. doi: 10.1162/089892903321208105 CrossRefPubMedGoogle Scholar
  59. Self MW, Zeki S (2005) The integration of colour and motion by the human visual brain. Cereb Cortex 15(8):1270–1279. doi: 10.1093/cercor/bhi010 CrossRefPubMedGoogle Scholar
  60. Spinelli L, Andino SG, Lantz G, Seeck M, Michel CM (2000) Electromagnetic inverse solutions in anatomically constrained spherical head models. Brain Topogr 13(2):115–125CrossRefPubMedGoogle Scholar
  61. Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127(4):355–370CrossRefPubMedGoogle Scholar
  62. Thirioux B, Mercier MR, Jorland G, Berthoz A, Blanke O (2010) Mental imagery of self-location during spontaneous and active self-other interactions: an electrical neuroimaging study. J Neurosci 30(21):7202–7214. doi: 10.1523/JNEUROSCI.3403-09.2010 CrossRefPubMedGoogle Scholar
  63. Thirioux B, Mercier MR, Blanke O, Berthoz A (2014) The cognitive and neural time course of empathy and sympathy: an electrical neuroimaging study on self-other interaction. Neuroscience 267:286–306. doi: 10.1016/j.neuroscience.2014.02.024 CrossRefPubMedGoogle Scholar
  64. Tononi G, Sporns O, Edelman GM (1992) Reentry and the problem of integrating multiple cortical areas: simulation of dynamic integration in the visual system. Cereb Cortex 2(4):310–335CrossRefPubMedGoogle Scholar
  65. Tootell RB, Taylor JB (1995) Anatomical evidence for MT and additional cortical visual areas in humans. Cereb Cortex 5(1):39–55CrossRefPubMedGoogle Scholar
  66. Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15(4):3215–3230PubMedGoogle Scholar
  67. Tootell RB, Dale AM, Sereno MI, Malach R (1996) New images from human visual cortex. Trends Neurosci 19(11):481–489CrossRefPubMedGoogle Scholar
  68. Ungerleider LG, Haxby JV (1994) ‘What’ and ‘where’ in the human brain. Curr Opin Neurobiol 4(2):157–165CrossRefPubMedGoogle Scholar
  69. Vaina LM (1989) Selective impairment of visual motion interpretation following lesions of the right occipito-parietal area in humans. Biol Cybern 61(5):347–359CrossRefPubMedGoogle Scholar
  70. Vaina LM, Gross CG (2004) Perceptual deficits in patients with impaired recognition of biological motion after temporal lobe lesions. Proc Natl Acad Sci USA 101(48):16947–16951. doi: 10.1073/pnas.0407668101 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Vaina LM, Soloviev S, Bienfang DC, Cowey A (2000) A lesion of cortical area V2 selectively impairs the perception of the direction of first-order visual motion. Neuroreport 11(5):1039–1044CrossRefPubMedGoogle Scholar
  72. Vaina LM, Sikoglu EM, Soloviev S, LeMay M, Squatrito S, Pandiani G, Cowey A (2010) Functional and anatomical profile of visual motion impairments in stroke patients correlate with fMRI in normal subjects. J Neuropsychol 4(Pt 2):121–145. doi: 10.1348/174866409X471760 CrossRefPubMedGoogle Scholar
  73. Vanduffel W, Fize D, Peuskens H, Denys K, Sunaert S, Todd JT, Orban GA (2002) Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 298(5592):413–415. doi: 10.1126/science.1073574 CrossRefPubMedGoogle Scholar
  74. Wang J, Zhou T, Qiu M, Du A, Cai K, Wang Z, Zhou C, Meng M, Zhuo Y, Fan S, Chen L (1999) Relationship between ventral stream for object vision and dorsal stream for spatial vision: an fMRI + ERP study. Hum Brain Mapp 8(4):170–181. doi: 10.1002/(SICI)1097-0193(1999)8:4<170:AID-HBM2>3.0.CO;2-W CrossRefPubMedGoogle Scholar
  75. Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Shipp S, Zeki S (1993) Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex 3(2):79–94CrossRefPubMedGoogle Scholar
  76. Zhuang J, Peltier S, He S, LaConte S, Hu X (2008) Mapping the connectivity with structural equation modeling in an fMRI study of shape-from-motion task. Neuroimage 42(2):799–806. doi: 10.1016/j.neuroimage.2008.05.036 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Manuel R. Mercier
    • 1
    • 2
    • 3
    • 6
  • Sophie Schwartz
    • 4
    • 5
  • Laurent Spinelli
    • 3
  • Christoph M. Michel
    • 2
  • Olaf Blanke
    • 1
    • 3
    • 7
  1. 1.Laboratory of Cognitive Neuroscience, Brain-Mind InstituteEcole Polytechnique Fédérale de Lausanne (EPFL)LausanneSwitzerland
  2. 2.The Functional Brain Mapping Laboratory, Department of NeuroscienceUniversity of GenevaGenevaSwitzerland
  3. 3.Department of NeurologyUniversity HospitalGenevaSwitzerland
  4. 4.Department of Fundamental NeuroscienceUniversity of GenevaGenevaSwitzerland
  5. 5.Swiss Center for Affective SciencesUniversity of GenevaGenevaSwitzerland
  6. 6.Centre de Recherche Cerveau et Cognition (CerCo), CNRS, UMR5549, Pavillon Baudot CHU PurpanToulouse CedexFrance
  7. 7.Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics and Brain Mind InstituteSwiss Federal Institute of Technology (EPFL)GenevaSwitzerland

Personalised recommendations