The development of audiovisual multisensory integration across childhood and early adolescence: A high-density electrical mapping study

Cerebral Cortex

Volumn 21, Issue 5, 2011, Pages 1042-1055

  Brandwein, Alice B ^a,b,c   Foxe, John J ^a,b,c   Russo, Natalie N ^a,b   Altschuler, Ted S ^a,b   Gomes, Hilary ^b,c   Molholm, Sophie ^a,b  

^a Children's Evaluation and Rehabilitation Center   (United States)

^b Departments of Psychology and Biology ^*  (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

children; cross modal; development, electrophysiology; ERP; multisensory integration

Indexed keywords

ADOLESCENT; ARTICLE; AUDIOVISUAL MULTISENSORY INTEGRATION; CHILD; CHILD BEHAVIOR; EVENT RELATED POTENTIAL; FEMALE; HEARING; HUMAN; MALE; NERVE CELL PLASTICITY; NORMAL HUMAN; PRIORITY JOURNAL; RESPONSE TIME; VISION;

ACOUSTIC STIMULATION; ADOLESCENT; ADULT; AGING; AUDITORY CORTEX; AUDITORY PERCEPTION; BRAIN MAPPING; CHILD; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; NEOCORTEX; NERVE NET; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL PERCEPTION; YOUNG ADULT;

EID: 79954573497     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq170     Document Type: Article

References (76)

1. Anderson P. 2002. Assessment and development of executive function (EF) during childhood. Child Neuropsychol. 8:71-82. (Pubitemid 36246261)
2. Anderson RA, Snyder LH, Bradley DC, Xing J. 1997. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu Rev Neurosci. 20:303-330. (Pubitemid 27106384)
3. Bahrick LE, Hernandez-Reif M, Flom R. 2005. Development of infant learning about specific face-voice relations. Dev Psychol. 41:541-542.
4. Bair WN, Kiemel T, Jeka JJ, Clark JE. 2007. Development of multisensory reweighting for posture control in children. Exp Psychol. 183:435-446. (Pubitemid 350029361)
5. Barutchu A, Crewther DP, Crewther SG. 2009. The race that precedes coactivation: development of multisensory facilitation in children. Dev Sci. 12:464-473.
6. Barutchu A, Danaher J, Crewther SG, Innes-Brown H, Shivdasani MN, Paolini AG. 2009. Audiovisual integration in noise by children and adults. J Exp Child Psychol. 105:38-50.
7. Benoit MM, Raij T, Lin FH, Jaaskelainen IP, Stufflemeam S. 2010. Primary and multisensory cortical activity is correlated with audiovisual percepts. Hum Brain Mapp. 31:526-538.
8. Calvert GA. 2001. Crossmodal processing brain: insights from functional neuroimaging studies. Cereb Cortex. 11:1110-1123. (Pubitemid 33108238)
9. Carriere B, Royal DW, Perrault TJ, Morrison SP, Vaughan JW, Stein BE, Wallace MT. 2007. Visual deprivation alters the development of cortical multisensory integration. J Neurophysiol. 98:2858-2867. (Pubitemid 350127944)
10. Ceponiene R, Rinne R, Naatanen R. 2002. Maturation of cortical sound processing as indexed by event-related potentials. Clin Neurophysiol. 113:870-882. (Pubitemid 34621193)
11. Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA. 2002. Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp. 15:95-111. (Pubitemid 34123736)
12. Doniger GM, Foxe JJ, Schroeder CE, Murray MM, Higgins BA, Javitt DC. 2001. Visual perceptual learning in human object based recognition areas: a repetition priming study using high-density electrical mapping. Neuroimage. 13:305-313. (Pubitemid 34185019)
13. Doniger GM, Silipo G, Rabinowicz EF, Snodgrass JG, Javitt DC. 2001. Impaired sensory processing as a basis for object-recognition deficits in schizophrenia. Am J Psychiatry. 158:1818-1826. (Pubitemid 33054774)
14. Fitch RH, Tallal P. 2003. Neural mechanisms of language-based learning impairments: insights from human populations and animal models. Behav Cogn Neurosci Rev. 2:155-178.
15. Forster B, Cavina-Pratesi C, Aglioti SM, Berlucchi G. 2002. Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time. Exp Brain Res. 143:480-487. (Pubitemid 34253297)
16. Foxe JJ, Morocz IA, Murray MM, Higgins BA, Javitt DC, Schroeder CE. 2000. Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res Cogn Brain Res. 10:77-83.
17. Foxe JJ, Simpson GV. 2002. Flow of activation from V1 to frontal cortex in humans. A framework for defining "early" visual processing. Exp Brain Res. 142:139-150. (Pubitemid 34028247)
18. Fry AF, Hale S. 2000. Relationships among processing speed, working memory, and fluid intelligence in children. Biol Psychol. 54:1-34.
19. Giard MH, Peronnet F. 1999. Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci. 11:473-490. (Pubitemid 29520540)
20. Gomes H, Dunn M, Ritter W, Kurtzberg D, Brattson A, Kreuzer JA, Vaughan HG. 2001. Spatiotemporal maturation of the central and lateral N1 components to tones. Dev Brain Res. 129:147-155. (Pubitemid 32744778)
21. Gondan M, Niederhaus B, Rosler F, Roder B. 2005. Multisensory processing in the redundant-target effect: a behavioral and eventrelated potential study Percept Psychophys. 67:713-726. (Pubitemid 41328715)
22. Gori M, Del Viva M, Sandini G, Burr D. 2008. Young children do not integrate visual and haptic form information. Curr Biol. 18:694-698.
23. Harrington LK, Peck CK. 1998. Spatial disparity affects visual-auditory interactions in human sensorimotor processing. Exp Brain Res. 122:247-252. (Pubitemid 28414358)
24. Hughes H, Reuter-Lorenz PA, Nozawa G, Fendrich R. 1994. Visualauditory interactions in sensorimotor processing: saccades versus manual responses. J Exp Psychol Human. 20:131-153.
25. Kail R. 1991. Developmental change in speed of processing during childhood and adolescence. Psychol Bull. 109:490-501.
26. Kim S, James TW. 2010. Enhanced effectiveness in visuo-haptic objectselective brain regions with increasing stimulus salience. Hum Brain Mapp. 31:678-693.
27. Kohl PK, Meltzoff AN. 1982. The bimodal perception of speech in infancy. Science. 218:1138-1141.
28. Konrad K, Neufang S, Theil CM, Specht K, Hanisch C, Fan J, Herpertz-Dahlmann B, Fink GR. 2005. Development of attentional networks: an fMRI study with children and adults. Neuroimage. 28:429-439. (Pubitemid 41443512)
29. Kuefner D, de Heering A,Jacques C, Palmero-Soler E, Rossion B. 2010. Early visual evoked electrophysiological responses over the human brain (P1, N170) show stable patterns of face-sensitivity from 4 years to adulthood. Front Hum Neurosci. 3:1-22.
30. Leavitt VM, Molholm S, Ritter W, Shpaner M, Foxe JJ. 2007. Auditory processing in schizophrenia during the middle latency period (10-50 ms): high-density electrical mapping and source analysis reveal subcortical antecedents to early cortical deficits. J Psychiatry Neurosci. 3:339-353. (Pubitemid 47492759)
31. Leitman DI, Hoptman MJ, Foxe JJ, Saccente E, Wylie GR, Nierenberg J, Jalbrzikowski M, Lim KO, Javitt DC. 2007. The neural substrates of impaired prosodic detection in schizophrenia and its sensorial antecedents. Am J Psychiatry. 164:474-482. (Pubitemid 46513162)
32. Lewkowicz DJ. 1992. Infants' responsiveness to the auditory and visual attributes of a sounding/moving stimulus. Percept Psychophys. 52:519-528.
33. Lewkowicz DJ, Ghazanfar AA. 2009. The emergence of multisensory systems through perceptual narrowing. Trends Cogn Sci. 13:470-478.
34. Lewkowicz DL. 2002. Heterogeneity and heterochrony in the development of intersensory perception. Brain Res Cogn Brain Res. 14:41-63.
35. Lippe S, Roy MS, Perchet C, Lassonde M. 2007. Electrophysiological markers ofvisuocortical development. Cereb Cortex. 17:100-107.
36. Lovelace CT, Stein BE, Wallace MT. 2003. An irrelevant light enhances auditory detection in humans: a psychophysical analysis of multisensory integration in stimulus detection. Brain Res Cogn Brain Res. 17:447-453. (Pubitemid 36860069)
37. Luciana M, Conklin HM, Hooper CJ, Yarger RS. 2005. The development of nonverbal working memory and executive control processes in adolescents. Child Dev. 76:697-712. (Pubitemid 40747175)
38. Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA. 2004. Maturation of cognitive processes from late childhood to early adulthood. Child Dev. 75:1357-1372. (Pubitemid 39442885)
39. Macaluso E, Eimer M, Frith CD, Driver J. 2003. Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms. Exp Brain Res. 149:62-74. (Pubitemid 36286816)
40. Maravita A, Bolognini N, Bricolo E, Marzi CA, Savazzi S. 2008. Is audiovisual integration subserved by the superior colliculus in humans? Neuroreport. 19:271-275. (Pubitemid 351322961)
41. Miller JO. 1982. Divided attention: evidence for coactivation with redundant signals. Cogn Psychol. 13:247-279.
42. Miller JO. 1986. Time course of coactivation in bimodal divided attention. Percept Psychophys. 40:331-343.
43. Molholm S, Ritter W, Javitt D, Foxe J. 2004. Multisensory visual-auditory object recognition in humans: a high-density electrical mapping study. Cereb Cortex. 14:452-465. (Pubitemid 38506976)
44. Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ. 2002. Multisensory auditory-visual interactions during early sensory processing in humans: a high density electrical mapping study. Cogn Brain Res. 14:115-128. (Pubitemid 34626802)
45. Molholm S, Sehatpour P, Mehta AD, Shpaner M, Gomez-Ramirez M, Ortigue S, Dyke J, Schwartz TH, Foxe JJ. 2006. Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings. J Neurophysiol. 96:721-729. (Pubitemid 44155212)
46. Moore JK, Linthicum F. 2007. The human auditory system: a timeline of development. Int J Audiol. 46:460-478. (Pubitemid 350194919)
47. Moran RJ, Molholm S, Reilly RB, Foxe JJ. 2008. Changes in effective connectivity of human superior parietal lobule under multisensory and unisensory stimulation. Eur J Neurosci. 27:2303-2312. (Pubitemid 351590899)
48. Mullette-Gillman OA, Cohen YE, Groh JM. 2009. Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. Cereb Cortex. 19:1761-1775.
49. Murray MM, Foxe JJ, Higgins BA, Javitt DC, Schroedrer CE. 2001. Visuospatial response interactions in early cortical processing during a simple reaction time task: a high density electrical mapping study. Neuropsychologia. 39:828-844. (Pubitemid 32455003)
50. Murray MM, Foxe JJ, Wylie GR. 2005. The brain uses single-trial multisensory memories to discriminate without awareness. Neuroimage. 27:473-478. (Pubitemid 41074847)
51. Murray MM, Imber ML,Javitt DC, Foxe JJ. 2006. Boundary completion is automatic and dissociable from shape discrimination. J Neurosci. 26:12043-12054. (Pubitemid 44772115)
52. Murray MM, Molholm S, Michel CM, Ritter W, Heslenfeld DJ, Schroeder CE, Javitt DC, Foxe JJ. 2005. Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low level sensory cortices are not constrained by stimulus alignment. Cereb Cortex. 15:963-974. (Pubitemid 40848065)
53. Naatanen R, Picton T. 1987. The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology. 24:375-425. (Pubitemid 17114207)
54. Neil PA, Chee-Ruiter C, Scheier C, Lewkowicz DJ, Shimojo S. 2006. Development of multisensory spatial integration and perception in humans. Dev Sci. 9:454-464. (Pubitemid 44179903)
55. Patterson ML, Werker JF. 2003. Two-month-old infants match phonetic information in lips and voice. Dev Sci. 6:191-196. (Pubitemid 36420229)
56. Paus T, Babenko V, Radil T. 1990. Development of an ability to maintain verbally instructed central gaze fixation studied in 8-to 10-year-old children. Int J Psychophysiol. 10:53-61. (Pubitemid 20374361)
57. Ponton CW, Eggermont JJ, Kwong B, Don M. 2000. Maturation of human central auditory system activity: evidence from multi-channel evoked potentials. Clin Neurophysiol. 111:220-236. (Pubitemid 30009436)
58. Posner MI, Rothbar MK. 1998. Attention, self-regulation and conscious-ness. Philos Trans R Soc Lond B Biol Sci. 35:1915-1927.
59. Ross LA, Molholm S, Gomez-Ramirez M, Sehatpour P, Brandwein AB, Russo N, Gomes H, Saint-Amour D, Foxe JJ. 2008. Audiovisual integration in word recognition in typically developing children and children with autistic spectrum disorder. International multisensory research forum. Hamburg (Germany).
60. Ross LA Saint-Amour D, Leavitt VM, Javitt DC, Foxe JJ. 2007. Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments. Cereb Cortex. 17:1147-1153. (Pubitemid 46598855)
61. Ross LA, Saint-Amour D, Leavitt VM, Molholm S, Javitt DC, Foxe JJ. 2007. Impaired multisensory processing in schizophrenia: deficits in the visual enhancement of speech comprehension under noisy envi-ronmental conditions. Schizophr Res. 97:173-183. (Pubitemid 350088394)
62. Russo N, Foxe JJ, Brandwein AB, Altschuler T, Gomes H, Molholm S. 2010. Multisensory processing in children with autism: high-density electrical mapping of auditory-somatosensory integration. Autism Res. 3:1-15.
63. Stanford TR, Stein BE. 2007. Superadditivity in multisensory integration: putting the computation in context. Neuroreport. 18:787-792. (Pubitemid 46686028)
64. Stein BE, Burr D, Constantinidis C, Laurienti PJ, Meredith MA, Perrault TJ, Ramachandran R, Roder B, Rowland BA, Satian K, et al. 2010. Semantic confusion regarding the development of multisen-sory integration: a practical solution. Eur J Neurosci. 31:1713-1720.
65. Stein BE, Labos E, Kruger L. 1973. Sequence ofchanges in properties of neurons of superior colliculus of the kitten during maturation. J Neurophysiol. 36:667-679.
66. Talsma D, Woldorff MG. 2005. Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J Cogn Neurosci. 17:1098-1114. (Pubitemid 41045581)
67. Teder-Salejarvi WA, McDonald JJ, Di Russo F, Hillyard SA. 2002. An analysis of audio-visual crossmodal integration by means of eventrelated potential (ERP) recordings. Brain Res Cogn Brain Res. 14:106-114. (Pubitemid 34626801)
68. Teder-Salejarvi WA, Munte T, Sperlich F, Hillyard SA. 1999. Intra-modal and cross-modal spatial attention to auditory and visual stimuli. An event-related brain potential study. Brain Res Cogn Brain Res. 8:327-343. (Pubitemid 29518317)
69. Wallace MT, Carriere BN, Perrault TJ, Vaughan JW, Stein BE. 2006. The development of cortical multisensory integration. J Neurosci. 26:11844-11849. (Pubitemid 44772094)
70. Wallace MT, Perrault TJ, Hairston WD, Stein BE. 2004. Visual experience is necessary for the development of multisensory integration. J Neurosci. 24:9580-9584. (Pubitemid 39441512)
71. Wallace MT, Stein BE. 1997. Development ofmultisensory neurons and multisensory integration in cat superior colliculus. J Neurosci. 17:2429-2444. (Pubitemid 27137410)
72. Wallace MT, Stein BE. 2007. Early experience determines how the senses will interact. J Neurophysiol. 97:921-926. (Pubitemid 46143406)
73. Welsh MC, Pennington BF, Groisser DB. 1991. A normative-developmental study of executive function: a window on prefrontal function in children. Dev Neuropsychol. 7:131-149.
74. Werner S, Noppeney U. 2010. Distinct functional contributions of primary sensory and association areas to audiovisual integration in object categorization. J Neurosci. 30:2662-2675.
75. Wylie GR, Javitt DC, Foxe JJ. 2003. Task switching: a high density electrical mapping study. Neuroimage. 20:2322-2342. (Pubitemid 37543643)
76. Yu L, Rowland BA, Stein BE. 2010. Initiating the development of multisensory integration by manipulating sensory experience. J Neurosci. 30:4904-4913.