Representation of head-centric flow in the human motion complex

Journal of Neuroscience

Volumn 26, Issue 21, 2006, Pages 5616-5627

  Goossens, Jeroen ^a,b   Dukelow, Sean P ^c   Menon, Ravi S ^d   Vilis, Tutis ^c   Van Den Berg, Albert V ^e  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d ROBARTS RESEARCH INSTITUTE   (Canada)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Head movements; Heading; Optic flow; Pursuit eye movements; Reference frames; Spatial perception; Vestibular

Indexed keywords

ARTICLE; CONTROLLED STUDY; EYE MOVEMENT; EYE TRACKING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAD MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; MONKEY; NORMAL HUMAN; PRIORITY JOURNAL; RETINA; SIGNAL TRANSDUCTION; TEMPORAL CORTEX; VISION; VISUAL STIMULATION; ADULT; BRAIN MAPPING; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; EVOKED MUSCLE RESPONSE; EVOKED VISUAL RESPONSE; METHODOLOGY; MOTOR CORTEX; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; TEMPORAL LOBE; VISUAL CORTEX; VISUAL FIELD;

ADULT; BRAIN MAPPING; EVOKED POTENTIALS, MOTOR; EVOKED POTENTIALS, VISUAL; EYE MOVEMENTS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; TEMPORAL LOBE; VISUAL CORTEX; VISUAL FIELDS; VISUAL PERCEPTION;

EID: 33745000095     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0730-06.2006     Document Type: Article

References (69)

1. Bardy BG, Warren Jr WH (1997) Visual control of braking in goal-directed action and sport. J Sports Sci 15:607-620.
2. Barton JJ, Simpson T, Kiriakopoulos E, Stewart C, Crawley A, Cuthrie B, Wood M, Mikulis D (1996) Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception. Ann Neurol 40:387-398.
3. Beintema JA, van den Berg AV (1998) Heading detection using motion templates and eye velocity gain fields. Vision Res 38:2155-2179.
4. Beintema JA, van den Berg AV (2001) Pursuit affects precision of perceived heading for small viewing apertures. Vision Res 41:2375-2391.
5. Bradley DC, Maxwell M, Andersen RA, Banks MS, Shenoy KV (1996) Mechanisms of heading perception in primate visual cortex. Science 273:1544-1547.
6. Bremmer F, Ilg UJ, Thiele A, Distler C, Hoffmann KP (1997) Eye position effects in monkey cortex. I. Visual and pursuit-related activity in extrastriate areas MT and MST. J Neurophysiol 77:944-961.
7. Britten KH, van Wezel RJ (1998) Electrical microstimulation of cortical area MST biases heading perception in monk. Nat Neurosci 1:59-63.
8. Chawla D, Phillips J, Buechel C, Edwards R, Friston KJ (1998) Speed-dependent motion-sensitive responses in V5: an fMRI study. NeuroImage 7:86-96.
9. Churchland AK, Lisberger SG (2005) Relationship between extraretinal component of firing rate and eye speed in area MST of macaque monkeys. J Neurophysiol 94:2416-2426.
10. Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol (Lond) 351:217-250.
11. Collewijn H, Tamminga EP (1986) Human fixation and pursuit in normal and open-loop conditions: effects of central and peripheral retinal targets. J Physiol (Lond) 379:109-129.
12. Collewijn H, van der Mark F, Jansen TC (1975) Precise recording of human eye movements. Vision Res 15:447-450.
13. Crowell JA, Banks MS, Shenoy KV, Andersen RA (1998) Visual self-motion perception during head turns. Nat Neurosci 1:732-737.
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 117:1039-1054.
15. Desimone R, Ungerleider LG (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164-189.
16. DeSouza JF, Dukelow SP, Vilis T (2002) Eye position signals modulate early dorsal and ventral visual areas. Cereb Cortex 12:991-997.
17. Duffy CJ, Wurtz RH (1991) Sensitivity of MST neurons to optic flow stimuli. II. A continuum of response selectivity to large-field stimuli. J Neurophysiol 65:1329-1345.
18. Dukelow SP, DeSouza JF, Culham JC, van den Berg AV, Menon RS, Vilis T (2001) Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. J Neurophysiol 86:1991-2000.
19. Dumoulin SO, Bittar RG, Kabani NJ, Baker Jr CL, Le Goualher G, Buce Pike G, Evans AC (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10:454-463.
20. Dupont P, Orban GA, De Bruyn B, Verbruggen A, Mortelmans L (1994) Many areas in the human brain respond to visual motion. J Neurophysiol 72:1420-1424.
21. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647.
22. Gibson JJ (1966) The perception of the visual world. Boston, MA: Houghton Mifflin.
23. 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 10:1563-1573.
24. Goltz HC, DeSouza JF, Menon RS, Tweed DB, Vilis T (2003) Interaction of retinal image and eye velocity in motion perception. Neuron 39:569-576.
25. Graziano MSA, Andersen RA, Snowden RJ (1994) Tuning of MST neurons to spiral motions. J Neurosci 14:54-67.
26. Hanada M (2005) An algorithmic model of heading perception. Biol Cybern 92:8-20.
27. Huk AC, Heeger DJ (2002) Pattern-motion responses in human visual cortex. Nat Neurosci 5:72-75.
28. Huk AC, Dougherty RF, Heeger DJ (2002) Retinotopy and functional subdivision of human areas MT and MST. J Neurosci 22:7195-7205.
29. Ilg UJ, Schumann S, Thier P (2004) Posterior parietal cortex neurons encode target motion in world-centered coordinates. Neuron 43:145-151.
30. Koenderink JJ (1986) Optic flow. Vision Res 26:161-179.
31. Koenderink JJ, van Doorn AJ (1987) Facts on optic flow. Biol Cybern 56:247-254.
32. Lappe M (1998) A model of the combination of optic flow and extraretinal eye movement signals in primate extrastriate visual cortex. Neural Net 11:742-744.
33. Lappe M, Bremmer F, Pekel M, Thiele A, Hoffman K-P (1996) Optic flow processing in monkey STS: a theoretical and experimental approach. J Neurosci 16:6265-6285.
34. Lappe M, Bremmer F, van den Berg AV (1999) Perception of self-motion from visual flow. Trends Cogn Sci 3:329-336.
35. Maunsell JH, van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563-2586.
36. McCarthy G, Spicer M, Adrignolo A, Luby M, Gore J, Allison T (1995) Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans. Hum Brain Map 2:234-243.
37. Morrone MC, Tosetti M, Montanaro D, Fiorentini A, Cioni G, Burr DC (2000) A cortical area that responds specifically to optic flow, revealed by fMRI. Nat Neurosci 3:1322-1328.
38. Orban GA, Lagae L, Verri A, Raiguel S, Xiao D, Maes H, Torre V (1992) First-order analysis of optical flow in monkey brain. Proc Natl Acad Sci USA 89:2595-2599.
39. Orban GA, Fize D, Peuskens H, Denys K, Nelissen K, Sunaert S, Todd J, Vanduffel W (2003) Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI. Neuropsychologia 41:1757-1768.
40. Page WK, Duffy CJ (1999) MST neuronal responses to heading direction during pursuit eye movements. J Neurophysiol 81:596-610.
41. Page WK, Duffy CJ (2003) Heading representation in MST: sensory interactions and population encoding. J Neurophysiol 89:1994-2013.
42. Perrone JA (1992) Model for the computation of self-motion in biological systems. J Opt Soc Am 9:177-194.
43. Petit L, Haxby JV (1999) Functional anatomy of pursuit eye movements in humans as revealed by fMRI. J Neurophysiol 82:463-471.
44. Peuskens H, Sunaert S, Dupont P, Van Hecke P, Orban GA (2001) Human brain regions involved in heading estimation. J Neurosci 21:2451-2461.
45. Rees G, Friston K, Koch C (2000) A direct quantitative relationship between the functional properties of human and macaque V5. Nat Neurosci 3:716-723.
46. Regan D, Beverley KI (1982) How do we avoid confounding the direction we are looking with the direction we are moving? Science 215:194-196.
47. Royden CS, Banks MS, Crowell JA (1992) The perception of heading during eye movements. Nature 360:583-585.
48. Royden CS, Crowell JA, Banks MS (1994) Estimating heading during eye movements. Vision Res 34:3197-3214.
49. Shenoy KV, Bradley DC, Andersen RA (1999) Influence of gaze rotation on the visual response of primate MSTd neurons. J Neurophysiol 81:2764-2786.
50. Shenoy KV, Crowell JA, Andersen RA (2002) Pursuit speed compensation in cortical area MSTd. J Neurophysiol 88:2630-2647.
51. Smith AT, Greenlee MW, Singh KD, Kraemer FM, Henning 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.
52. Strupp JP (1996) Stimulate: a GUI-based fMRI analysis software package. NeuroImage 3:S607.
53. Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127:355-370.
54. Talairach J, Tournoux P (1988) Co-Planar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. Stuttgart, Germany: Thieme Medical Publishers.
55. Tanabe J, Tregellas J, Miller D, Ross RG, Freedman R (2002) Brain activation during smooth-pursuit eye movements. NeuroImage 17:1315-1324.
56. Thier P, Erickson RG (1992) Responses of visual-tracking neurons from cortical area MST-I to visual, eye and head motion. Eur J Neurosci 4:539-553.
57. Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Brady JT, Rosen BR (1995a) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375:139-141.
58. Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995b) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15:3215-3230.
59. Upadhyay UD, Page WK, Duffy CJ (2000) MST responses to pursuit across optic flow with motion parallax. J Neurophysiol 84:818-826.
60. van den Berg AV (1992) Robustness of perception of heading from optic flow. Vision Res 32:1285-1296.
61. van den Berg AV (1996) Judgements of heading. Vision Res 36:2337-2350.
62. van den Berg AV, Beintema JA (2000) The mechanism of interaction between visual flow and eye velocity signals for heading perception. Neuron 26:747-752.
63. van den Berg AV, Beintema JA, Frens MA (2001) Heading and path percepts from visual flow and eye pursuit signals. Vision Res 41:3467-3486.
64. van den Berg AV, van Ee R, Noest AJ (2005) Mixed visual reference frames: perceiving nonretino-centric visual quantities in a retino-centric frame. Proceedings of the International Society for Optical Engineering, Human Vision and Electronic Imaging X, Vol 5666 (Rogowitz BE, Pappas TN, Daly SJ, eds), pp 449-461. Bellingham, WA: SPIE.
65. Warren Jr WH (1995) Self-motion: visual perception and visual control. In: Perception of space and motion. San Diego: Academic.
66. Warren Jr WH, Hannon DJ (1988) Direction of self-motion is perceived from optical flow. Nature 336:162-163.
67. 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 3:79-94.
68. Zeki S, Watson JD, Lueck CJ, Friston KJ, Kennard C, Frackowiak RS (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11:641-649.
69. Zemel RS, Sejnowski TJ (1998) A model for encoding multiple object motions and self-motion in area MST of primate visual cortex. J Neurosci 18:531-547.