The brain network underlying the recognition of hand gestures in the blind: The supramodal role of the extrastriate body area

Journal of Neuroscience

Volumn 34, Issue 30, 2014, Pages 10096-10108

  Kitada, Ryo ^a,b   Yoshihara, Kazufumi ^c   Sasaki, Akihiro T ^d,e   Hashiguchi, Maho ^a,b   Kochiyama, Takanori ^f   Sadato, Norihiro ^a,b,g  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e RIKEN   (Japan)

^f ATR Brain Activity Imaging Center   (Japan)

^g UNIVERSITY OF FUKUI   (Japan)

Author keywords

EBA; FMRI; Haptics; Touch

Indexed keywords

ACCURACY; ADULT; AGE; ARTICLE; AUTOMATED PATTERN RECOGNITION; BLINDNESS; CONTROLLED STUDY; EBA LOCALIZER TASK; EXTRASTRIATE BODY AREA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND GESTURE RECOGNITION; HAPTIC OBJECT IDENTIFICATION TASK; HUMAN; HUMAN EXPERIMENT; MAJOR CLINICAL STUDY; MALE; NERVE CELL NETWORK; NEUROIMAGING; PRIORITY JOURNAL; TASK PERFORMANCE; VISUAL CORTEX; VISUAL DEPRIVATION; VISUAL OBJECT IDENTIFICATION TASK; VISUAL STIMULATION; VISUAL SYSTEM FUNCTION;

EBA; FMRI; HAPTICS; TOUCH;

ADULT; BLINDNESS; BRAIN; FEMALE; GESTURES; HAND; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PSYCHOMOTOR PERFORMANCE; RECOGNITION (PSYCHOLOGY); VISUAL CORTEX; YOUNG ADULT;

EID: 84904552775     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0500-14.2014     Document Type: Article

References (65)

1. Amedi A, Raz N, Pianka P, Malach R, Zohary E (2003) Early 'visual' cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 6:758-766. CrossRef Medline
2. Amedi A, Floel A, Knecht S, Zohary E, Cohen LG (2004) Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat Neurosci 7:1266-1270. CrossRef Medline
3. Amedi A, Stern WM, Camprodon JA, Bermpohl F, Merabet L, Rotman S, Hemond C, Meijer P, Pascual-Leone A (2007) Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat Neurosci 10:687-689. CrossRef Medline
4. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95-113. CrossRef Medline
5. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839-851. CrossRef Medline
6. Astafiev SV, Stanley CM, Shulman GL, Corbetta M (2004) Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat Neurosci 7:542-548. CrossRef Medline
7. Bedny M, Konkle T, Pelphrey K, Saxe R, Pascual-Leone A (2010) Sensitive period for a multimodal response in human visual motion area MT/MST. Curr Biol 20:1900-1906. CrossRef Medline
8. Burton H, Snyder AZ, Conturo TE, Akbudak E, Ollinger JM, Raichle ME (2002a) Adaptive changes in early and late blind: a fMRI study of Braille reading. J Neurophysiol 87:589-607. Medline
9. Burton H, Snyder AZ, Diamond JB, Raichle ME (2002b) Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. J Neurophysiol 88:3359-3371. CrossRef Medline
10. Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8-16. CrossRef Medline
11. Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Falz L, Dambrosia J, Honda M, Sadato N, Gerloff C, Catalá MD, Hallett M (1997) Functional relevance of cross-modal plasticity in blind humans. Nature 389:180-183. CrossRef Medline
12. Collignon O, Vandewalle G, Voss P, Albouy G, Charbonneau G, Lassonde M, Lepore F (2011) Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans. Proc Natl Acad Sci U S A 108:4435-4440. CrossRef Medline
13. Costantini M, Urgesi C, Galati G, Romani GL, Aglioti SM (2011) Haptic perception and body representation in lateral and medial occipitotemporal cortices. Neuropsychologia 49:821-829. CrossRef Medline
14. Dettmers C, Fink GR, Lemon RN, Stephan KM, Passingham RE, Silbersweig D, Holmes A, Ridding MC, Brooks DJ, Frackowiak RS (1995) Relation between cerebral activity and force in the motor areas of the human brain. J Neurophysiol 74:802-815. Medline
15. Downing PE, Jiang Y, Shuman M, Kanwisher N (2001) A cortical area selective for visual processing of the human body. Science 293:2470-2473. CrossRef Medline
16. Downing PE, Wiggett AJ, Peelen MV (2007) Functional magnetic resonance imaging investigation of overlapping lateral occipitotemporal activations using multi-voxel pattern analysis. J Neurosci 27:226-233. CrossRef Medline
17. Friston KJ, Jezzard P, Turner R (1994) Analysis of functional MRI timeseries. Hum Brain Mapp 1:153-171. CrossRef
18. Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1996) Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4:223-235. CrossRef Medline
19. Friston KJ, Glaser DE, Henson RN, Kiebel S, Phillips C, Ashburner J (2002) Classical and Bayesian inference in neuroimaging: applications. Neuroimage 16:484-512. CrossRef Medline
20. Friston KJ, Penny WD, Glaser DE (2005) Conjunction revisited. Neuroimage 25:661-667. CrossRef Medline
21. Friston KJ, Ashburner J, Kiebel SJ, Nichols TE, Penny WD (2007) Statistical parametric mapping: the analysis of functional brain images. London: Academic.
22. Fuke S, Ogino M, Asada M (2007) Body image constructed from motor and tactile images with visual information. Int J Hum Robot 4:347-364. CrossRef
23. Greenough WT, Black JE, Wallace CS (1987) Experience and brain development. Child Dev 58:539-559. CrossRef Medline
24. Grol MJ, Majdandziæ J, Stephan KE, Verhagen L, Dijkerman HC, Bekkering H, Verstraten FA, Toni I (2007) Parieto-frontal connectivity during visually guided grasping. J Neurosci 27:11877-11887. CrossRef Medline
25. He C, Peelen MV, Han Z, Lin N, Caramazza A, Bi Y (2013) Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience. Neuroimage 79:1-9. CrossRef Medline
26. Holmes AP, Friston KJ (1998) Generalisability, random effects and population inference. Neuroimage 7:S754.
27. Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7:942-951. CrossRef Medline
28. Jackson PL, Meltzoff AN, Decety J (2006) Neural circuits involved in imitation and perspective-taking. Neuroimage 31:429-439. CrossRef Medline
29. Kitada R, Johnsrude IS, Kochiyama T, Lederman SJ (2009) Functional specialization and convergence in the occipito-temporal cortex supporting haptic and visual identification of human faces and body parts: an fMRI study. J Cogn Neurosci 21:2027-2045. CrossRef Medline
30. Kitada R, Johnsrude IS, Kochiyama T, Lederman SJ (2010) Brain networks involved in haptic and visual identification of facial expressions of emotion: an fMRI study. Neuroimage 49:1677-1689. CrossRef Medline
31. Kitada R, Okamoto Y, Sasaki AT, Kochiyama T, Miyahara M, Lederman SJ, Sadato N (2013) Early visual experience and the recognition of basic facial expressions: involvement of the middle temporal and inferior frontal gyri during haptic identification by the early blind. Front Hum Neurosci 7:7. CrossRef Medline
32. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI (2009) Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci 12:535-540. CrossRef Medline
33. Lederman SJ, Klatzky RL (1987) Hand movements: a window into haptic object recognition. Cogn Psychol 19:342-368. CrossRef Medline
34. Leppänen JM, Nelson CA (2009) Tuning the developing brain to social signals of emotions. Nat Rev Neurosci 10:37-47. CrossRef Medline
35. Mahon BZ, Anzellotti S, Schwarzbach J, Zampini M, Caramazza A (2009) Category-specific organization in the human brain does not require visual experience. Neuron 63:397-405. CrossRef Medline
36. + is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals. Brain Res Bull 82:264-270. CrossRef Medline
37. Meltzoff AN (2005) Imitation and other minds: the 'like me' hypothesis. In: Perspectives on imitation: from cognitive neuroscience to social science (Hurley S, Chater N, eds), pp 55-77. Cambridge: Massachusetts Institute of Technology.
38. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25. CrossRef Medline
39. Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653-660. CrossRef Medline
40. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113. CrossRef Medline
41. Oosterhof NN, Wiggett AJ, Diedrichsen J, Tipper SP, Downing PE (2010) Surface-based information mapping reveals crossmodal vision-action representations in human parietal and occipitotemporal cortex. J Neurophysiol 104:1077-1089. CrossRef Medline
42. Orlov T, Makin TR, Zohary E (2010) Topographic representation of the human body in the occipitotemporal cortex. Neuron 68:586-600. CrossRef Medline
43. Peelen MV, Downing PE (2005a) Within-subject reproducibility of category-specific visual activation with functional MRI. Hum Brain Mapp 25:402-408. CrossRef Medline
44. Peelen MV, Downing PE (2005b) Selectivity for the human body in the fusiform gyrus. J Neurophysiol 93:603-608. CrossRef Medline
45. Peelen MV, Bracci S, Lu X, He C, Caramazza A, Bi Y (2013) Tool selectivity in left occipitotemporal cortex develops without vision. J Cogn Neurosci 25:1225-1234. CrossRef Medline
46. Pietrini P, Furey ML, Ricciardi E, Gobbini MI, Wu WH, Cohen L, Guazzelli M, Haxby JV (2004) Beyond sensory images: object-based representation in the human ventral pathway. Proc Natl Acad Sci U S A 101:5658-5663. CrossRef Medline
47. Poirier C, Collignon O, Scheiber C, Renier L, Vanlierde A, Tranduy D, Veraart C, De Volder AG (2006) Auditory motion perception activates visual motion areas in early blind subjects. Neuroimage 31:279-285. CrossRef Medline
48. Reich L, Szwed M, Cohen L, Amedi A (2011) A ventral visual stream reading center independent of visual experience. Curr Biol 21:363-368. CrossRef Medline
49. Renier LA, Anurova I, De Volder AG, Carlson S, VanMeter J, Rauschecker JP (2010) Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind. Neuron 68:138-148. CrossRef Medline
50. +. Cereb Cortex 17: 2933-2939. CrossRef Medline
51. Ricciardi E, Bonino D, Sani L, Vecchi T, Guazzelli M, Haxby JV, Fadiga L, Pietrini P (2009) Do we really need vision? How blind people "see" the actions of others. J Neurosci 29:9719-9724. CrossRef Medline
52. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TE (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426-428. CrossRef Medline
53. Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661-670. CrossRef Medline
54. Sadato N, Pascual-Leone A, Grafman J, Ibañez V, Deiber MP, Dold G, Hallett M (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526-528. CrossRef Medline
55. Sadato N, Ibañez V, Campbell G, Deiber MP, Le Bihan D, Hallett M (1997) Frequency-dependent changes of regional cerebral blood flow during finger movements: functional MRI compared to PET. J Cereb Blood Flow Metab 17:670-679. CrossRef Medline
56. Sadato N, Okada T, Honda M, Yonekura Y (2002) Critical period for crossmodal plasticity in blind humans: a functional MRI study. Neuroimage 16:389-400. CrossRef Medline
57. Shattuck DW, Mirza M, Adisetiyo V, Hojatkashani C, Salamon G, Narr KL, Poldrack RA, Bilder RM, Toga AW (2008) Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage 39:1064-1080. CrossRef Medline
58. Spiridon M, Fischl B, Kanwisher N (2006) Location and spatial profile of category-specific regions in human extrastriate cortex. Hum Brain Mapp 27:77-89. CrossRef Medline
59. Striem-Amit E, Amedi A (2014) Visual cortex extrastriate body-selective area activation in congenitally blind people "seeing" by using sounds. Curr Biol 24:687-692. CrossRef Medline
60. Striem-Amit E, Dakwar O, Reich L, Amedi A (2012) The large-scale organization of "visual" streams emerges without visual experience. Cereb Cortex 22:1698-1709. CrossRef Medline
61. 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 15:3215-3230. Medline
62. Wager TD, Nichols TE (2003) Optimization of experimental design in fMRI: a general framework using a genetic algorithm. Neuroimage 18: 293-309. CrossRef Medline
63. +, and visual field maps to parcellate limbselective activations in human lateral occipitotemporal cortex. Neuroimage 56:2183-2199. CrossRef Medline
64. Wolbers T, Klatzky RL, Loomis JM, Wutte MG, Giudice NA (2011) Modality-independent coding of spatial layout in the human brain. Curr Biol 21:984-989. CrossRef Medline
65. Worsley KJ, Friston KJ (1995) Analysis of fMRI time-series revisited-again. Neuroimage 2:173-181. CrossRef Medline