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. 1998 Dec 29;7(1):67–77. doi: 10.1002/(SICI)1097-0193(1999)7:1<67::AID-HBM6>3.0.CO;2-K

Perception of first‐ and second‐order motion: Separable neurological mechanisms?

Lucia M Vaina 1,3, Alan Cowey 2, David Kennedy 1,3
PMCID: PMC6873310  PMID: 9882091

Abstract

An unresolved issue in visual motion perception is how distinct are the processes underlying “first‐order” and “second‐order” motion. The former is defined by spatiotemporal variations of luminance and the latter by spatiotemporal variations in other image attributes, such as contrast or depth. Here we describe two neurological patients with focal unilateral lesions whose contrasting perceptual deficits on psychophysical tasks of “first‐order” and “second‐order” motion are related to the maps of the human brain established by functional neuroimaging and gross anatomical features. We used a relatively fine‐grained neocortical parcellation method applied to high‐resolution MRI scans of the patients' brains to illustrate a subtle, yet highly specific dissociation in the visual motion system in humans. Our results suggest that the two motion systems are mediated by regionally separate mechanisms from an early stage of cortical processing. Hum. Brain Mapping. 7:67–77, 1999. © 1999 Wiley‐Liss, Inc.

Keywords: Visual motion deficits, neurological patients, first and second order motion, cortical parcellation

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REFERENCES

  1. Albright TD. 1992. Form‐cue invariant motion processing in primate visual cortex. Science 255:1141–1143. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=92188190&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  2. Boulton JC, Baker CL. 1993. Different parameters control motion perception above and below a critical density. Vision Res 33:1803–1811. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94090966&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  3. Boussaoud D, Ungerleider LG, Desimone R. 1990. Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol 296:462–495. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90293225&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  4. Caviness VS Jr, Makris N, Meyer J, Kennedy DN. 1996. MRI‐based parcellation of human neocortex: An anatomically specified method with estimate of reliability. Cereb Cortex 6:726–736. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97079475&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  5. Chubb C, Sperling G. 1988. Drift‐balanced random stimuli: A general basis for studying non‐Fourier motion perception. J Opt Soc Am A 5:1986–2007. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=89094576&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  6. Clarke S, Miklossy J. 1990. Occipital cortex in man: Organization of callosal connections, related myelo‐and cytoarchitecture, and putative boundaries of functional visual areas. J Comp Neurol 298:188–214. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=91009962&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  7. Clifford WGC, Vaina LM. 1998. A computational model of selective deficits in first‐ and second‐order motion processing. Vision Res; (in press). [DOI] [PubMed] [Google Scholar]
  8. De Yoe EA, Carman G, Bandettini PA, Glickman S, Cox R, Miller D, Neitz J. 1996. Mapping striate and extrastriate visual areas in human cerebral cortex. Proc Natl Acad Sci USA 93:2382–2386. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96197321&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dupont P, Orban GA, De Bruyn B, Verbruggen A, Mortelmans L. 1994. Many areas in the human hrain respond to visual motion. J Neurophysiol 72(3):1420–1424. [DOI] [PubMed] [Google Scholar]
  10. Engel SA, Glover GH, Wandell BA. 1997. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97242831&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  11. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47. [DOI] [PubMed] [Google Scholar]
  12. Filipek PA, Richelme C, Kennedy DN, Verne J, Caviness S. 1994. The young adult human brain: An MRI‐based morphometric analysis. Cereb Cortex 4(4):344–260. [DOI] [PubMed] [Google Scholar]
  13. Greenlee MW, Smith AT. 1997. Detection and discrimination of first‐ and second‐order motion in patients with unilateral brain damage. J Neurosci 17:804–818. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=98007489&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ledgeway T, Smith AT. 1994. Evidence for separate motion‐detecting mechanisms for first‐ and second‐order motion in human vision. Vision Res 34:2727–2740. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95065758&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  15. Lu ZL, Sperling G. 1995. The functional architecture of human visual motion perception. Vision Res 35:2697–2722. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96048222&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  16. Newsome WT, Pare EB. 1988. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=88258617&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. O'Keefe LP, Movshon JA. 1996. Processing of first‐ and second‐order motion signals by neurons in area MT of the macaque monkey. Vis Neurosci 15:305–317. [DOI] [PubMed] [Google Scholar]
  18. O'Keefe LP, Carandini M, Beusmans JMH, Movshon JA. 1993. MT neuronal responses to 1st‐ and 2nd‐order motion. Soc Neurosci Abstr 19:1283. [Google Scholar]
  19. Orban GA, Dupont P, De Bruyn B, Vogels R, Vandenberghe R, Mortelmans L. 1995. A motion area in human visual cortex. Proc Natl Acad Sci USA 92:993–997. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95166818&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Plant GT, Laxer KD, Barbaro NM, Schiffman JS, Nakayama K. 1993. Impaired visual motion perception in the contralateral hemifield following unilateral posterior cerebral lesions. Brain 116:1337–1353. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94123070&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  21. Rademacher J, Galaburda AM, Kennedy DN, Filipek PA, Caviness VS. 1992. Human cerebral cortex: Localization, parcellation, and morphometry with magnetic resonance imaging. J Cogn Neurosci 4(4):352–374. [DOI] [PubMed] [Google Scholar]
  22. Saiviroporoon P. 1992. A computerized instrument for the diagnosis of visual deficits in humans. M.S. Thesis, Department of Biomedical Engineering, Boston University.
  23. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RBH. 1995. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95273966&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  24. Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J. 1998. The processing of first‐ and second‐order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). J Neurosci 18:3816–3830. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=98237759&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Somers DC, Seiffert AE, Dale AM, Tootell RBH. 1998. fMRI analysis of second‐order visual motion perception and attentive tracking. NeuroImage 7:S323. [Google Scholar]
  26. Talairach J, Tournoux P. 1988. Co‐Planar Sterotaxic Atlas of the Human Brain. New York: Georg Thieme Verlag. [Google Scholar]
  27. Tootell RBH, Reppas JB, Kwong KK, Mallach 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):3215–3230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tootell RBH, Dale AM, Sereno MI, Malach, R. 1996. New images from human visual cortex. Trends Neurosci 19(11):481–489. [DOI] [PubMed] [Google Scholar]
  29. Tootell RBH, Hadjikhani NK, Mendola JD, Marrett S, Dale AM. 1998. From retinotopy to recognition: fMRI in human visual cortex. Trends Cogn Sci 2:174–183. [DOI] [PubMed] [Google Scholar]
  30. Ungerleider LG. 1996. What and where in the human brain? Evidence from human functional brain imaging studies In: Carminiti R, Hoffmann K‐P, Lacquanti F, Altman J, eds. Vision and Movement Mechanisms in the Cerebral Cortex Strasbourg: Human Frontiers Science Programme Organization; p 23–30. [Google Scholar]
  31. Vaina LM, Cowey A. 1996. Impairment of the perception of second order motion but not first order motion in a patient with unilateral focal brain damage. Proc Roy Soc Lond B 263:1225–1232. [DOI] [PubMed] [Google Scholar]
  32. Vaina LM, LeMay M. 1993. Deficits of non‐Fourier motion perception in a patient with normal performance on short‐range motion tasks. Soc Neurosci Abstr 19:1284. [Google Scholar]
  33. Vaina LM, Makris N, Kennedy D, Cowey A. 1996. The neuroanatomical damage producing selective deficits to first or second order motion in stroke patients provides further evidence for separate mechanisms. NeuroImage 3:S360. [Google Scholar]
  34. Vaina LM, Makris N, Kennedy D, Cowey A. 1998. The selective impairment of the perception of first‐order motion by unilateral cortical brain damage. Vis Neurosci 15:333–348. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=98266570&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  35. Watson JDG, Meyers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC. 1993. Area V5 of the human brain: Evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex 3:79–94. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=93257894&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  36. Werkhoven P, Sperling G, Chubb C. 1993. The dimensionality of texture‐defined motion: A single channel theory. Vision Res 33:463–486. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=93276609&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  37. Wilson HR, Ferrera VP, Yo C. 1992. A psychophysically motivated model for two‐dimensional motion perception. Vis Neurosci 9:79–97. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=92338124&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  38. Wurtz RH, Yamasaki DS, Duffy CJ, Roy JP. 1990. Functional specialization for visual motion processing in primate cerebral cortex. Cold Spring Harbor Symposium on Quantitative Biology, Volume LV, pp 717–727. [DOI] [PubMed]
  39. Zeki S, Watson JDG, Lueck CK, Friston KJ, Kennard C, Frackowiak RSJ, 1993. A direct demonstration of functional specialisation in human visual cortex. J Neurosci 11:641–649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zhou Y‐X, Baker CLB Jr. 1993. A processing stream in mammalian visual cortex neurons for non‐Fourier responses. Science 261:98–101. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=93303631&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]

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