Induced deficits in speed perception by transcranial magnetic stimulation of human cortical areas V5/MT+ and V3A

Journal of Neuroscience

Volumn 28, Issue 27, 2008, Pages 6848-6857

  McKeefry, Declan J ^a   Burton, Mark P ^a   Vakrou, Chara ^a   Barrett, Brendan T ^a   Morland, Anthony B ^b  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

fMRI; Psychophysics; Retinotopic mapping; Speed perception; Transcranial magnetic stimulation; V3A; V5 MT+

Indexed keywords

ADULT; ARTICLE; BLOOD OXYGENATION; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; BRAIN MAPPING; EVALUATION; HUMAN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; SPATIAL FREQUENCY DISCRIMINATION; STIMULUS RESPONSE; TRANSCRANIAL MAGNETIC STIMULATION; VELOCITY; VISUAL CORTEX; VISUAL STIMULATION; BRAIN CIRCULATION; ELECTROMAGNETIC FIELD; HISTOLOGY; MALE; METHODOLOGY; MOVEMENT PERCEPTION; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PERCEPTION DISORDER; PERCEPTIVE THRESHOLD; PHOTOSTIMULATION; PHYSIOLOGY; RADIATION EXPOSURE; RETINA; TIME; TIME PERCEPTION; VISUAL FIELD; VISUAL SYSTEM;

ADULT; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; ELECTROMAGNETIC FIELDS; HUMANS; MALE; MOTION PERCEPTION; NERVE NET; PERCEPTUAL DISORDERS; PHOTIC STIMULATION; RETINA; SENSORY THRESHOLDS; TIME FACTORS; TIME PERCEPTION; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 49049111175     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1287-08.2008     Document Type: Article

References (62)

1. Allen EA, Pasley BN, Duong T, Freeman RD (2007) Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317:1918-1921.
2. Anand S, Olson JD, Hotson JR (1998) Tracing the timing of human analysis of motion and chromatic signals from occipital to tempero-parietooccipital cortex: a transcranial magnetic stimulation study. Vision Res 38:2619-2627.
3. Beckers G, Hömberg V (1992) Cerebral visual motion blindness: transitory akinetopsia induced by transcranial magnetic stimulation of human area V5. Proc Biol Sci 249:173-178.
4. Beckers G, Zeki S (1995) The consequences of inactivating areas V1 and V5 on visual motion perception. Brain 118:49-60.
5. Bisley JW, Paternak T (2000) The multiple roles of cortical areas MT/MST in remembering the direction of visual motion. Cereb Cortex 10:1053-1065.
6. Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207-4221.
7. Campana G, Cowey A, Walsh V (2002) Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb Cortex 12:663-669. 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.
8. Churchland MM, Lisberger SG (2001) Shifts in the population response in the middle temporal visual area parallel perceptual and motor illusions produced by apparent motion. J Neurosci 21:9387-9402.
9. Cowey A (2005) The Ferrier Lecture: What can transcranial magnetic stimulation tell us about how the brain works? Philos Trans R Soc Lond B Biol Sci 360:1185-1205.
10. Cowey A, Campana G, Walsh V, Vaina LM (2006) The role of human extrastriate visual areas V5/MT and V2/V3 in the perception of the direction of global motion: a transcranial magnetic stimulation study. Exp Brain Res 171:558-562.
11. DeYoe EA, Carman GJ, Bandettini P, Glickman S, Wieser J, Cox R, Miller D, Neitz J (1996) Mapping striate and extra-striate visual areas in human cerebral cortex. Proc Natl Acad Sci U S A 93:2382-2386.
12. 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.
13. 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.
14. Harris JA, Clifford CW, Miniussi C (2008) The functional effect of transcranial magnetic stimulation: signal suppression or neural noise generation? J Cogn Neurosci 20:734-740.
15. Hotson J, Braun D, Herzberg W, Boman D (1994) Transcranial magnetic stimulation of extra-striate cortex degrades human motion direction discrimination. Vision Res 34:2115-2123.
16. Huk AC, Heeger DJ (2000) Task-related modulation of visual cortex. J Neurophysiol 83:3525-3536.
17. Kahana MJ, Sekuler R (2002) Recognizing spatial patterns: a noisy exemplar approach. Vision Res 42:2177-2192.
18. Komatsu H, Wurtz RH (1989) Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J Neurophysiol 62:31-47.
19. Krekelberg B, van Wezel RJ, Albright TD (2006a) Adaptation in macaque MT reduces perceived speed and improves speed discrimination. J Neurophysiol 95:255-270.
20. Krekelberg B, van Wezel RJ, Albright TD (2006b) Interactions between speed and contrast tuning in the middle temporal area: implications for the neural code for speed. J Neurosci 26:8988-8998.
21. Lagae L, Raiguel S, Orban GA (1993) Speed and direction sensitivity of macaque middle temporal neurons. J Neurophysiol 69:19-39.
22. Laycock R, Crewther DP, Fitzgerald PB, Crewther SG (2007) Evidence for fast signals and later processing in human V1/V2 and V5/MT+: a TMS study of motion perception. J Neurophysiol 98:1253-1262.
23. Liu J, Newsome WT (2005) Correlation between speed perception and neural activity in the middle temporal visual area. J Neurosci 25:711-722.
24. Liu J, Newsome WT (2006) Local field potential in cortical area MT: stimulus tuning and behavioral correlations. J Neurosci 26:7779-7790.
25. Liu J, Wandell BA (2005) Specializations for chromatic and temporal signals in human visual cortex. J Neurosci 25:3459-3468.
26. Matthews N, Luber B, Qian N, Lisanby SH (2001) Transcranial magnetic stimulation differentially affects speed and direction judgments. Exp Brain Res 140:397-406.
27. Maunsell JH, Van Essen DC (1983) Functional properties of neurons in the middle temporal visual area of the macaque monkey. J Neurophysiol 49:1127-1147.
28. McKee SP, Silverman GH, Nakayama K (1986) Precise velocity discrimination despite random variations in temporal frequency and contrast. Vision Res 26:609-619.
29. McKeefry DJ, Watson JD, Frackowiak RS, Fong K, Zeki S (1997) The activity in human areas V1, V2, V3 and V5 during the perception of coherent and incoherent motion. Neuroimage 5:1-12.
30. Merabet L, Desautels A, Minville K, Casanova C (1998) Motion integration in a thalamic visual nucleus. Nature 396:265-268.
31. Morgan MJ, Watamaniuk SN, McKee SP (2000) The use of an implicit standard for measuring discrimination thresholds. Vision Res 40:2341-2349.
32. Newsome WT, Paré EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201-2211.
33. Nover H, Anderson CH, DeAngelis GC (2005) A logarithmic, scale-invariant representation of speed in macaque middle temporal area accounts for speed discrimination performance. J Neurosci 25:10049-10060.
34. Orban GA, Saunders RC, Vandenbussche E (1995) Lesions of the superior temporal cortical motion areas impair speed discrimination in the macaque monkey. Eur J Neurosci 7:2261-2276.
35. Pascual-Leone A, Walsh V (2001) Fast backprojections from the motion to the primary visual area are necessary for visual awareness. Science 292:510-512.
36. Pascual-Leone A, Walsh V, Rothwell J (2000) Transcranial magnetic stimulation in cognitive neuroscience - virtual lesion, chronometry and functional connectivity. Curr Opin Neurobiol 10:232-237.
37. Perrone JA, Thiele A (2001) Speed skills: measuring the visual speed analyzing properties of primate MT neurons. Nat Neurosci 4:526-532.
38. Priebe NJ, Lisberger SG (2004) Estimating target speed from the population response in visual area MT. J Neurosci 24:1907-1916.
39. Priebe NJ, Cassanello CR, Lisberger SG (2003) The neural representation of speed in macaque area MT/V5. J Neurosci 23:5650-5661.
40. Priebe NJ, Lisberger SG, Movshon JA (2006) Tuning for spatiotemporal frequency and speed in directionally selective neurons of macamque striate cortex. J Neurosci 26:2941-2950.
41. 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.
42. Rodman HR, Albright TD (1987) Coding of visual stimulus velocity in area MT of the macaque. Vision Res 27:2035-2048.
43. Sack AT, Kohler A, Linden DE, Goebel R, Muckli L (2006) The temporal characteristics of motion processing in hMT/V5+: combining fMRI and neuronavigated TMS. Neuroimage 29:1326-1335.
44. Seiffert AE, Somers DC, Dale AM, Tootell RBH (2003) Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects. Cereb Cortex 13:340-349.
45. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple human visual areas in humans revealed by functional MRI. Science 268:889-893.
46. Shipp S, Zeki S (1989) The organization of connections between areas V5 and V1 in macaque monkey visual cortex. Eur J Neurosci 1:309-332.
47. Silvanto J, Muggleton NG, Cowey A, Walsh V (2007a) Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur J Neurosci 25:1874-1881.
48. Silvanto J, Muggleton NG, Cowey A, Walsh V (2007b) Neural activation state determines behavioural susceptibility to modified theta burst transcranial magnetic stimulation. Eur J Neurosci 26:523-528.
49. Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123-1128.
50. 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.
51. Sunaert S, Van Hecke P, Marchal G, Orban GA (2000) Attention to speed of motion, speed discrimination, and task difficulty: an fMRI study. Neuroimage 11:612-623.
52. Teo PC, Sapiro G, Wandell BA (1997) Creating connected representations of cortical gray matter for functional MRI visualization. IEEE Trans Med Imaging 16:852-863.
53. Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995a) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15:3215-3230.
54. Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Brady TJ, Rosen BR (1995b) Visual motion after-effect in human cortical area MT/V5 revealed by functional magnetic resonance imaging. Nature 375:139-141.
55. Tootell RB, Mendola JD, Hadjikhani NK, Ledden PJ, Liu AK, Reppas JB, Sereno MI, Dale AM (1997) Functional analysis of V3A and related areas in human visual cortex. J Neurosci 17:7060-7078.
56. Villeneuve MY, Kupers R, Gjedde A, Ptito M, Casanova C (2005) Patternmotion selectivity in the human pulvinar. Neuroimage 28:474-480.
57. Walsh V, Cowey A (2000) Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci 1:73-79.
58. Walsh V, Ellison A, Battelli L, Cowey A (1998) Task-specific impairments and enhancements induced by magnetic stimulation of human visual area V5. Proc Biol Sci 265:537-543.
59. Wandell BA, Chial S, Backus BT (2000) Visualization and measurement of the cortical surface. J Cogn Neurosci 12:739-752.
60. Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Transcranial Magnetic Stimulation. Electroencephalogr Clin Neurophysiol 108:1-16.
61. 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.
62. Zeki S, Perry RJ, Bartels A (2003) The processing of kinetic contours in the brain. Cereb Cortex 13:189-202.