Multisensory integration mechanisms during aging

Frontiers in Human Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Freiherr, Jessica ^a   Lundström, Johan N ^b,c,d   Habel, Ute ^a   Reetz, Kathrin ^a,e,f  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MONELL CHEMICAL SENSES CENTER   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^f FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Aging neuroscience; Cognition; Crossmodal sensory integration; Elderly population; Multimodal; Multisensory integration

Indexed keywords

AGE; AGING; ALZHEIMER DISEASE; BRAIN FUNCTION; BRAIN REGION; BRAIN SIZE; DEFAULT MODE NETWORK; HUMAN; INFORMATION PROCESSING; MULTISENSORY INTEGRATION; RESTING STATE NETWORK; REVIEW; SENSORY DYSFUNCTION;

EID: 84890499789     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00863     Document Type: Review

References (78)

1. Andrews-Hanna, J. R., Snyder, A. Z., Vincent, J. L., Lustig, C., Head, D., Raichle, M. E., et al. (2007). Disruption of large-scale brain systems in advanced aging. Neuron 56, 924-935. doi: 10.1016/j.neuron.2007.10.038
2. Beauchamp, M. S., Yasar, N. E., Frye, R. E., and Ro, T. (2008). Touch, sound and vision in human superior temporal sulcus. Neuroimage 41, 1011-1020. doi: 10.1016/j.neuroimage.2008.03.015
3. Bradley, K. M., O'sullivan, V. T., Soper, N. D., Nagy, Z., King, E. M., Smith, A. D., et al. (2002). Cerebral perfusion SPET correlated with Braak pathological stage in Alzheimer's disease. Brain 125, 1772-1781. doi: 10.1093/brain/awf185
4. Bremmer, F., Schlack, A., Shah, N. J., Zafiris, O., Kubischik, M., Hoffmann, K., et al. (2001). Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29, 287-296. doi: 10.1016/s0896-6273(01)00198-2
5. Browndyke, J. N., Giovanello, K., Petrella, J., Hayden, K., Chiba-Falek, O., Tucker, K. A., et al. (2013). Phenotypic regional functional imaging patterns during memory encoding in mild cognitive impairment and Alzheimer's disease. Alzheimers Dement. 9, 284-294. doi: 10.1016/j.jalz.2011.12.006
6. Calvert, G. A. (2001). Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb. Cortex 11, 1110-1123. doi: 10. 1093/cercor/11.12.1110
7. Chen, Y. C., and Spence, C. (2011). Crossmodal semantic priming by naturalistic sounds and spoken words enhances visual sensitivity. J. Exp. Psychol. Hum. Percept. Perform. 37, 1554-1568. doi: 10.1037/a0024329
8. Chetelat, G., Desgranges, B., Landeau, B., Mezenge, F., Poline, J. B., De La Sayette, V., et al. (2008). Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. Brain 131, 60-71. doi: 10. 1093/brain/awm288
9. Dalton, P., Doolittle, N., Nagata, H., and Breslin, P. A. (2000). The merging of the senses: integration of subthreshold taste and smell. Nat. Neurosci. 3, 431-432. doi: 10.1038/74797
10. Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S., and Cabeza, R. (2008). Que PASA? The posterior-anterior shift in aging. Cereb. Cortex 18, 1201-1209. doi: 10.1093/cercor/bhm155
11. Dematte, L. M., Sanabria, D., and Spence, C. (2006). Cross-modal associations between odors and colors. Chem. Senses 31, 531-538. doi: 10. 1093/chemse/bjj057
12. Dematte, M. L., Sanabria, D., and Spence, C. (2009). Olfactory discrimination: when vision matters? Chem. Senses 34, 103-109. doi: 10.1093/chemse/bjn055
13. Diaconescu, A. O., Hasher, L., and McIntosh, R. A. (2013). Visual dominance and multisensory integration changes with age. Neuroimage 65, 152-166. doi: 10.1016/j.neuroimage.2012.09.057
14. Diederich, A., Colonius, H., and Schomburg, A. (2008). Assessing age-related multisensory enhancement with the time-window-of-integration model. Neuropsychologia 46, 2556-2562. doi: 10.1016/j.neuropsychologia.2008.03. 026
15. Ethofer, T., Pourtois, G., and Wildgruber, D. (2006). Investigating audiovisual integration of emotional signals in the human brain. Prog. Brain Res. 156, 345-361. doi: 10.1016/s0079-6123(06)56019-4
16. Fabiani, M. (2012). It was the best of times, it was the worst of times: a psychophysiologist's view of cognitive aging. Psychophysiology 49, 283-304. doi: 10.1111/j.1469-8986.2011.01331.x
17. Falkenstein, M., Yordanova, J., and Kolev, V. (2006). Effects of aging on slowing of motor-response generation. Int. J. Psychophysiol. 59, 22-29. doi: 10.1016/j.ijpsycho.2005.08.004
18. Ferri, C. P., Prince, M., Brayne, C., Brodaty, H., Fratiglioni, L., Ganguli, M., et al. (2005). Global prevalence of dementia: a Delphi consensus study. Lancet 366, 2112-2117. doi: 10.1016/s0140-6736(05)67889-0
19. Filippi, M., and Agosta, F. (2011). Structural and functional network connectivity breakdown in Alzheimer's disease studied with magnetic resonance imaging techniques. J. Alzheimers Dis. 24, 455-474. doi: 10.3233/JAD-2011-101854
20. Gottfried, J. A., and Dolan, R. J. (2003). The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39, 375-386. doi: 10.1016/s0896-6273(03)00392-1
21. Grady, C. (2012). The cognitive neuroscience of ageing. Nat. Rev. Neurosci. 13, 491-505. doi: 10.1038/nrn3256
22. Grady, C. L., Maisog, J. M., Horwitz, B., Ungerleider, L. G., Mentis, M. J., Salerno, J. A., et al. (1994). Age-related changes in cortical blood flow activation during visual processing of faces and location. J. Neurosci. 14, 1450-1462.
23. Grady, C. L., Springer, M. V., Hongwanishkul, D., Mcintosh, A. R., and Winocur, G. (2006). Age-related changes in brain activity across the adult lifespan. J. Cogn. Neurosci. 18, 227-241. doi: 10.1162/jocn.2006.18.2.227
24. Gusnard, D. A., and Raichle, M. E. (2001). Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2, 685-694. doi: 10.1038/35094500
25. Hafkemeijer, A., Van Der Grond, J., and Rombouts, S. A. (2012). Imaging the default mode network in aging and dementia. Biochim. Biophys. Acta 1822, 431-441. doi: 10.1016/j.bbadis.2011.07.008
26. Hairston, W. D., Laurienti, P. J., Mishra, G., Burdette, J. H., and Wallace, M. T. (2003). Multisensory enhancement of localization under conditions of induced myopia. Exp. Brain Res. 152, 404-408. doi: 10.1007/s00221-003-1646-7
27. Hedman, A. M., Van Haren, N. E., Schnack, H. G., Kahn, R. S., and Hulshoff Pol, H. E. (2012). Human brain changes across the life span: a review of 56 longitudinal magnetic resonance imaging studies. Hum. Brain Mapp. 33, 1987-2002. doi: 10.1002/hbm.21334
28. Helfer, K. S. (1998). Auditory and auditory-visual recognition of clear and converational speech by older adults. J. Am. Acad. Audiol. 9, 234-242.
29. Hugenschmidt, C. E., Mozolic, J. L., and Laurienti, P. J. (2009). Suppression of multisensory integration by modality-specific attention in aging. Neuroreport 20, 349-353. doi: 10.1097/wnr.0b013e328323ab07
30. Kassuba, T., Klinge, C., Holig, C., Menz, M. M., Ptito, M., Roder, B., et al. (2011). The left fusiform gyrus hosts trisensory representations of manipulable objects. Neuroimage 56, 1566-1577. doi: 10.1016/j.neuroimage.2011.02.032
31. King, A. J., and Palmer, A. R. (1985). Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp. Brain Res. 60, 492-500. doi: 10.1007/bf00236934
32. Klasen, M., Chen, Y. H., and Mathiak, K. (2012). Multisensory emotions: perception, combination and underlying neural processes. Rev. Neurosci. 23, 381-392. doi: 10.1515/revneuro-2012-0040
33. Klasen, M., Kenworthy, C. A., Mathiak, K. A., Kircher, T. T., and Mathiak, K. (2011). Supramodal representation of emotions. J. Neurosci. 31, 13635-13643. doi: 10.1523/jneurosci.2833-11.2011
34. Kreifelts, B., Ethofer, T., Shiozawa, T., Grodd, W., and Wildgruber, D. (2009). Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice-and face-sensitive regions in the superior temporal sulcus. Neuropsychologia 47, 3059-3066. doi: 10.1016/j. neuropsychologia.2009.07.001
35. Langbaum, J. B., Chen, K., Lee, W., Reschke, C., Bandy, D., Fleisher, A. S., et al. (2009). Categorical and correlational analyses of baseline fluorodeoxyglucose positron emission tomography images from the Alzheimer's Disease Neuroimaging Initiative (ADNI). Neuroimage 45, 1107-1116. doi: 10.1016/j. neuroimage.2008.12.072
36. Langner, R., Kellermann, T., Eickhoff, S. B., Boers, F., Chatterjee, A., Willmes, K., et al. (2012). Staying responsive to the world: modality-specific and -nonspecific contributions to speeded auditory, tactile and visual stimulus detection. Hum. Brain Mapp. 33, 398-418. doi: 10.1002/hbm.21220
37. Laurienti, P. J., Burdette, J. H., Maldjian, J. A., and Wallace, M. T. (2006). Enhanced multisensory integration in older adults. Neurobiol. Aging 27, 1155-1163. doi: 10.1016/j.neurobiolaging.2005.05.024
38. Li, C. S., Yan, P., Bergquist, K. L., and Sinha, R. (2007). Greater activation of the "default" brain regions predicts stop signal errors. Neuroimage 38, 640-648. doi: 10.1016/j.neuroimage.2007.07.021
39. Liu, X. Z., and Yan, D. (2007). Ageing and hearing loss. J. Pathol. 211, 188-197. doi: 10.1002/path.2102
40. Mahoney, J. R., Li, P. C. C., Oh-Park, M., Verghese, J., and Holtzer, R. (2011). Multisensory integration across the senses in young and old adults. Brain Res. 1426, 43-53. doi: 10.1016/j.brainres.2011.09.017
41. Mahoney, J. R., Verghese, J., Dumas, K., Wang, C., and Holtzer, R. (2012). The effect of multisensory cues on attention in aging. Brain Res. 1472, 63-73. doi: 10.1016/j.brainres.2012.07.014
42. Meredith, M. A., and Stein, B. E. (1983). Interactions among converging sensory inputs in the superior colliculus. Science 221, 389-391. doi: 10.1126/science.6867718
43. Meredith, M. A., and Stein, B. E. (1985). Descending efferents form the superior colliculus relay integrated multisensory infromation. Science 227, 657-659. doi: 10.1126/science.3969558
44. Meredith, M. A., and Stein, B. E. (1986). Visual, auditory and somatosensory convergence on cells in superior colliculus results in multisensory integration. J. Neurophysiol. 56, 640-662.
45. Mozolic, J. L., Hugenschmidt, C. E., Peiffer, A. M., and Laurienti, P. J. (2008). Modality-specific selective attention attenuates multisensory integration. Exp. Brain Res. 184, 39-52. doi: 10.1007/s00221-007-1080-3
46. Mozolic, J. L., Hugenschmidt, C. E., Pfeiffer, A. M., and Laurienti, P. J. (2012). "Multisensory integration and aging," in The Neural Bases of Multisensory Processes, eds M. M. Murray and M. T. Wallace (Boca Raton, FL: CRC Press). http://www.ncbi.nlm.nih.gov/books/NBK92841/
47. Muller, V. I., Cieslik, E. C., Turetsky, B. I., and Eickhoff, S. B. (2012). Cross-modal interactions in audiovisual emotion processing. Neuroimage 60, 553-561. doi: 10.1016/j.neuroimage.2011.12.007
48. Muller, V. I., Habel, U., Derntl, B., Schneider, F., Zilles, K., Turetsky, B. I., et al. (2011). Incongruence effects in crossmodal emotional integration. Neuroimage 54, 2257-2266. doi: 10.1016/j.neuroimage.2010.10.047
49. Nordin, S., Almkvist, O., and Berglund, B. (2012). Is loss in odor sensitivity inevitable in the aging individual? A study of "successfully aged" elderly. Chem. Percept. 5, 188-196. doi: 10.1007/s12078-011-9102-8
50. Park, D. C., and Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 60, 173-196. doi: 10.1146/annurev.psych.59.103006.093656
51. Peiffer, A. M., Mozolic, J. L., Hugenschmidt, C. E., and Laurienti, P. J. (2007). Age-related multisensory enhancement in a simple audiovisual detection task. Neuroreport 18, 1077-1081. doi: 10.1097/wnr.0b013e3281e72ae7
52. Petrie, E. C., Cross, D. J., Galasko, D., Schellenberg, G. D., Raskind, M. A., Peskind, E. R., et al. (2009). Preclinical evidence of Alzheimer changes: convergent cerebrospinal fluid biomarker and fluorodeoxyglucose positron emission tomography findings. Arch. Neurol. 66, 632-637. doi: 10.1001/archneurol. 2009.59
53. Phillips, N. A., Baum, S., and Taler, V. (2009). "Audio-visual speech perception in mild cognitive impairment and healthy elderly controls", in AVSP 2009 - International Conference on Audio-Visual Speech Processing. Norwich, UK.
54. Price, J. L. (2008). Multisensory convergence in the orbital and ventrolateral prefrontal cortex. Chemosens. Percept. 1, 103-109. doi: 10.1007/s12078-008-9013-5
55. Rawson, N. E. (2006). Olfactory loss in aging. Sci. Aging Knowledge Environ. 2006:pe6. doi: 10.1126/sageke.2006.5.pe6
56. Raz, N., and Rodrigue, K. M. (2006). Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 30, 730-748. doi: 10.1016/j.neubiorev.2006.07.001
57. Reetz, K., Nickl-Jockschat, T., Kleiman, A., Schulz, J. B., Scheider, F., Laird, A. R., et al. (2012). Neuroanatomic changes and their association with cognitive decline in miled cognitive impairment: a meta-analysis. Brain Struct. Funct. 217, 115-125. doi: 10.1007/s00429-011-0333-x
58. Regenbogen, C., Schneider, D. A., Finkelmeyer, A., Kohn, N., Derntl, B., Kellermann, T., et al. (2012a). The differential contribution of facial expressions, prosody and speech content to empathy. Cogn. Emot. 26, 995-1014. doi: 10. 1080/02699931.2011.631296
59. Regenbogen, C., Schneider, D. A., Gur, R. E., Schneider, F., Habel, U., and Kellermann, T. (2012b). Multimodal human communication - Targeting facial expressions, speech content and prosody. Neuroimage 60, 2346-2356. doi: 10. 1016/j.neuroimage.2012.02.043
60. Sala, S., Agosta, F., Pagani, E., Copetti, M., Comi, G., and Filippi, M. (2012). Microstructural changes and atrophy in brain white matter tracts with aging. Neurobiol. Aging 33, 488-498, e482. doi: 10.1016/j.neurobiolaging.2010.04.027
61. Schlee, W., Leirer, V., Kolassa, S., Thurm, F., Elbert, T., and Kolassa, I. T. (2012). Development of large-scale functional networks over the lifespan. Neurobiol. Aging 33, 2411-2421. doi: 10.1016/j.neurobiolaging.2011.11.031
62. Schroeter, M. L., Stein, T., Maslowski, N., and Neumann, J. (2009). Neural correlates of Alzheimer's disease and mild cognitive impairment: a systematic and quantitative meta-analysis involving 1351 patients. Neuroimage 47, 1196-1206. doi: 10.1016/j.neuroimage.2009.05.037
63. Seo, H. S., and Hummel, T. (2011). Auditory-olfactory integration: congruent or pleasant sounds amplify odor pleasantness. Chem. Senses 36, 301-309. doi: 10.1093/chemse/bjq129
64. Seubert, J., Kellermann, T., Loughead, J., Boers, F., Brensinger, C., Schneider, F., et al. (2010a). Processing of disgusted faces is facilitated by odor primes: a functional MRI study. Neuroimage 53, 746-756. doi: 10.1016/j.neuroimage. 2010.07.012
65. Seubert, J., Loughead, J., Kellermann, T., Boers, F., Brensinger, C. M., and Habel, U. (2010b). Multisensory integration of emotionally valenced olfactory-visual information in patients with schizophrenia and healthy controls. J. Psychiatry Neurosci. 35, 185-194. doi: 10.1503/jpn.090094
66. Small, D. M., and Prescott, J. (2005). Odor/taste integration and the perception of flavor. Exp. Brain Res. 166, 345-357. doi: 10.1007/s00221-005-2376-9
67. Sommers, M. S., Tye-Murray, N., and Spehar, B. (2005). Auditory-visual speech perception and auditory-visual enhancement in normal-hearing younger and older adults. Ear Hear. 26, 263-275. doi: 10.1097/00003446-200506000-00003
68. Sowell, E. R., Thompson, P. M., and Toga, A. W. (2004). Mapping changes in the human cortex throughout the span of life. Neuroscientist 10, 372-392. doi: 10. 1177/1073858404263960
69. Spear, P. D. (1993). Neural bases of visual deficits during aging. Vision Res. 33, 2589-2609. doi: 10.1016/0042-6989(93)90218-l
70. Spence, C. (2011). Crossmodal correspondences: a tutorial review. Atten. Percept. Psychophys. 73, 971-995. doi: 10.3758/s13414-010-0073-7
71. Staal, J., Pinkney, L., and Roane, D. (2003). Assessment of stimulus preference in Snoezelen therapy for elderly with dementia. Br. J. Occup. Ther. 66, 542-551.
72. Stein, B. E., and Meredith, M. A. (1990). Multisensory integration. Neural and behavioral solutions for dealing with stimuli from different sensory modalities. Ann. N Y Acad. Sci. 608, 51-65. doi: 10.1111/j.1749-6632.1990.tb48891.x
73. Stein, B. E., and Stanford, T. R. (2008). Multisensory integration: current issues from the perspective of the single neuron. Nat. Rev. Neurosci. 9, 255-266. doi: 10. 1038/nrn2331
74. Stephen, J. M., Knoefel, J. E., Adair, J., Hart, B., and Aine, C. J. (2010). Aging-related changes in auditory and visual integration measured with MEG. Neurosci. Lett. 484, 76-80. doi: 10.1016/j.neulet.2010.08.023
75. Stine, E. A., Wingfield, A., and Myers, S. D. (1990). Age differences in processing information from television news: the effects of bisensory augmentation. J. Gerontol. 45, P1-P8. doi: 10.1093/geronj/45.1.p1
76. Walden, B. E., Busacco, D. A., and Montgomery, A. A. (1993). Benefit from visual cues in auditory-visual speech recognition by middle-aged and elderly persons. J. Speech Hear. Res. 36, 431-436.
77. Wang, L., Laviolette, P., O'keefe, K., Putcha, D., Bakkour, A., Van Dijk, K. R., et al. (2010a). Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals. Neuroimage 51, 910-917. doi: 10.1016/j.neuroimage.2010.02.046
78. Wang, L., Negreira, A., Laviolette, P., Bakkour, A., Sperling, R. A., and Dickerson, B. C. (2010b). Intrinsic interhemispheric hippocampal functional connectivity predicts individual differences in memory performance ability. Hippocampus 20, 345-351. doi: 10.1002/hipo.20771