Age differences in fMRI adaptation for sound identity and location

Frontiers in Human Neuroscience

Volumn , Issue MARCH, 2011, Pages

  Grady, Cheryl L ^a,b   Charlton, Rebecca ^c   He, Yu ^a   Alain, Claude ^a,b  

^a ROTMAN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Adaptation; Aging; Auditory system; FMRI; Spatial localization

Indexed keywords

ADULT; AGE DIFFERENCE; AGED; ARTICLE; AUDITORY ADAPTATION; AUDITORY SYSTEM FUNCTION; BRAIN FUNCTION; BRAIN REGION; COGNITION; CONTROLLED STUDY; DATA ANALYSIS; ENVIRONMENT; FEMALE; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING; HUMAN; HUMAN EXPERIMENT; MALE; PARIETAL CORTEX; POPULATION STRUCTURE; SOUND; SOUND DETECTION; SUBCORTEX; TEMPORAL CORTEX; TEMPORAL LOBE;

EID: 84933670525     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2011.00024     Document Type: Article

References (77)

1. Abel, S. M., Giguere, C., Consoli, A., and Papsin, B. C. (2000). The effect of aging on horizontal plane sound localization. J. Acoust. Soc. Am. 108, 743-752.
2. Aine, C. J., Adair, J. C., Knoefel, J. E., Hudson, D., Qualls, C., Kovacevic, S., Woodruff, C. C., Cobb, W., Padilla, D., Lee, R. R., and Stephen, J. M. (2005). Temporal dynamics of age-related differences in auditory incidental verbal learning. Brain Res. Cogn. Brain Res. 24, 1-18.
3. Alain, C., Arnott, S. R., Hevenor, S., Graham, S., and Grady, C. L. (2001). "What" and "where" in the human auditory system. Proc. Natl. Acad. Sci. U.S.A. 98, 12301-12306.
4. Alain, C., Shen, D., Yu, H., and Grady, C. L. (2010). Dissociable memory- and response-related activity in parietal cortex during auditory spatial working memory. Front. Psychol. 1:202. doi:10.3389/fpsyg.2010.00202
5. Alain, C., Yu, H., and Grady, C. (2008). The inferior parietal lobe contributes to auditory spatial working memory and sensorimotor integration. J. Cogn. Neurosci. 20, 285-295.
6. Altmann, C. F., Bledowski, C., Wibral, M., and Kaiser, J. (2007). Processing of location and pattern changes of natural sounds in the human auditory cortex. Neuroimage 35, 1192-1200.
7. Altmann, C. F., Henning, M., Doring, M. K., and Kaiser, J. (2008). Effects of feature-selective attention on auditory pattern and location processing. Neuroimage 41, 69-79.
8. Amedi, A., Malach, R., and Pascual-Leone, A. (2005). Negative BOLD differentiates visual imagery and perception. Neuron 48, 859-872.
9. Anderson, B., Mruczek, R. E., Kawasaki, K., and Sheinberg, D. (2008). Effects of familiarity on neural activity in monkey inferior temporal lobe. Cereb. Cortex 18, 2540-2552.
10. Belin, P., and Zatorre, R. J. (2003). Adaptation to speaker's voice in right anterior temporal lobe. Neuroreport 14, 2105-2109.
11. Buchel, C., Coull, J. T., and Friston, K. J. (1999). The predictive value of changes in effective connectivity for human learning. Science 283, 1538-1541.
12. Budd, T. W., Barry, R. J., Gordon, E., Rennie, C., and Michie, P. T. (1998). Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. Int. J. Psychophysiol. 31, 51-68.
13. Carp, J., Park, J., Polk, T. A., and Park, D. C. (in press). Age differences in neural distinctiveness revealed by multi-voxel pattern analysis. Neuroimage. doi: 10.1016/j.neuroimage.2010.04.267. [Epub ahead of print].
14. Chee, M. W., Goh, J. O., Venkatraman, V., Tan, J. C., Gutchess, A., Sutton, B., Hebrank, A., Leshikar, E., and Park, D. (2006). Age-related changes in object processing and contextual binding revealed using fMR adaptation. J. Cogn. Neurosci. 18, 495-507.
15. Cherry, K. E., Park, D. C., and Donaldson, H. (1993). Adult age differences in spatial memory: effects of structural context and practice. Exp. Aging Res. 19, 333-350.
16. Cranford, J. L., Andres, M. A., Piatz, K. K., and Reissig, K. L. (1993). Influences of age and hearing loss on the precedence effect in sound localization. J. Speech Hear. Res. 36, 437-441.
17. De Lucia, M., Cocchi, L., Martuzzi, R., Meuli, R. A., Clarke, S., and Murray, M. M. (2010). Perceptual and semantic contributions to repetition priming of environmental sounds. Cereb. Cortex 20, 1676-1684.
18. Deouell, L. Y., Heller, A. S., Malach, R., D'Esposito, M., and Knight, R. T. (2007). Cerebral responses to change in spatial location of unattended sounds. Neuron 55, 985-996.
19. Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proc. Natl. Acad. Sci. U.S.A. 93, 13494-13499.
20. Doehrmann, O., Naumer, M. J., Volz, S., Kaiser, J., and Altmann, C. F. (2008). Probing category selectivity for environmental sounds in the human auditory brain. Neuropsychologia 46, 2776-2786.
21. Efron, B., and Tibshirani, R. (1986). Bootstrap methods for standard errors, confidence intervals and other measures of statistical accuracy. Stat. Sci. 1, 54-77.
22. Fabiani, M., Low, K. A., Wee, E., Sable, J. J., and Gratton, G. (2006). Reduced suppression or labile memory? Mechanisms of inefficient filtering of irrelevant information in older adults. J. Cogn. Neurosci. 18, 637-650.
23. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). "Mini Mental State" - a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198.
24. Friston, K. (2005). A theory of cortical responses. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 360, 815-836.
25. Gazzaley, A., Cooney, J. W., Rissman, J., and D'Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nat. Neurosci. 8, 1298-1300.
26. Gilbert, J. R., Gotts, S. J., Carver, F. W., and Martin, A. (2010). Object repetition leads to local increases in the temporal coordination of neural responses. Front. Hum. Neurosci. 4:30. doi:10.3389/fnhum.2010.00030
27. Glover, G. H., and Lai, S. (1998). Self-navigated spiral fMRI: interleaved versus single-shot. Magn. Reson. Med. 39, 361-368.
28. Goh, J. O., Siong, S. C., Park, D., Gutchess, A., Hebrank, A., and Chee, M. W. (2004). Cortical areas involved in object, background, and object-background processing revealed with functional magnetic resonance adaptation. J. Neurosci. 24, 10223-10228.
29. Goh, J. O., Suzuki, A., and Park, D. C. (2010). Reduced neural selectivity increases fMRI adaptation with age during face discrimination. Neuroimage 51, 336-344.
30. Goodale, M. A., and Milner, A. D. (1992). Separate visual pathways for perception and action. Trends Neurosci. 15, 20-25.
31. Grady, C. L. (2002). Age-related differences in face processing: a meta-analysis of three functional neuroimaging experiments. Can. J. Exp. Psychol. 56, 208-220.
32. Grady, C. L., Yu, H., and Alain, C. (2008). Age-related differences in brain activity underlying working memory for spatial and nonspatial auditory information. Cereb. Cortex 18, 189-199.
33. Grill-Spector, K., Henson, R., and Martin, A. (2006). Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14-23.
34. Grill-Spector, K., Kushnir, T., Edelman, S., Avidan, G., Itzchak, Y., and Malach, R. (1999). Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24, 187-203.
35. Harms, M. P., and Melcher, J. R. (2002). Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. J. Neurophysiol. 88, 1433-1450.
36. Hasher, L., Zacks, R. T., and May, C. P. (1999). "Inhibitory control, circadian arousal, and age," in Attention and Performance XVII: Cognitive Regulation of Performance. Interaction of Theory and Application, eds D. Gopher and A. Koriat (Cambridge, MA: MIT Press), 653-675.
37. Head, D., and Isom, M. (2010). Age effects on wayfinding and route learning skills. Behav. Brain Res. 209, 49-58.
38. Healey, M. K., Campbell, K. L., and Hasher, L. (2008). "Cognitive aging and increased distractibility: costs and potential benefits," in Progress in Brain Research, Vol. 169, The Essence of Memory, eds W. S. Sossin, J.-C. Lacaille, V. F. Castellucci, and S. Belleville (Amsterdam: Elsevier), 353-363.
39. Inan, S., Mitchell, T., Song, A., Bizzell, J., and Belger, A. (2004). Hemodynamic correlates of stimulus repetition in the visual and auditory cortices: an fMRI study. Neuroimage 21, 886-893.
40. Joyce, C. A., Paller, K. A., McIsaac, H. K., and Kutas, M. (1998). Memory changes with normal aging: behavioral and electrophysiological measures. Psychophysiology 35, 669-678.
41. Kikuchi, Y., Horwitz, B., and Mishkin, M. (2010). Hierarchical auditory processing directed rostrally along the monkey's supratemporal plane. J. Neurosci. 30, 13021-13030.
42. Lawson, A. L., Guo, C., and Jiang, Y. (2007). Age effects on brain activity during repetition priming of targets and distracters. Neuropsychologia 45, 1223-1231.
43. Leventhal, A. G., Wang, Y., Pu, M., Zhou, Y., and Ma, Y. (2003). GABA and its agonists improved visual cortical function in senescent monkeys. Science 300, 812-815.
44. Li, L., Miller, E. K., and Desimone, R. (1993). The representation of stimulus familiarity in anterior inferior temporal cortex. J. Neurophysiol. 69, 1918-1929.
45. Lukic, A. S., Wernick, M. N., and Strother, S. C. (2002). An evaluation of methods for detecting brain activations from functional neuroimages. Artif. Intell. Med. 25, 69-88.
46. Maeder, P. P., Meuli, R. A., Adriani, M., Bellmann, A., Fornari, E., Thiran, J.-P., Pittet, A., and Clarke, S. (2001). Distinct pathways involved in sound recognition and localization: a human fMRI study. Neuroimage 14, 802-816.
47. McIntosh, A. R., Bookstein, F. L., Haxby, J. V., and Grady, C. L. (1996). Spatial pattern analysis of functional brain images using partial least squares. Neuroimage 3, 143-157.
48. McIntosh, A. R., Chau, W. K., and Protzner, A. B. (2004). Spatiotemporal analysis of event-related fMRI data using partial least squares. Neuroimage 23, 764-775.
49. McIntosh, A. R., and Lobaugh, N. L. (2004). Partial least squares analysis of neuroimaging data: applications and advances. Neuroimage 23(Suppl. 1), S250-S263.
50. McMahon, D. B., and Olson, C. R. (2007). Repetition suppression in monkey inferotemporal cortex: relation to behavioral priming. J. Neurophysiol. 97, 3532-3543.
51. Nenadic, I., Gaser, C., Volz, H. P., Rammsayer, T., Hager, F., and Sauer, H. (2003). Processing of temporal information and the basal ganglia: new evidence from fMRI. Exp. Brain Res. 148, 238-246.
52. Owsley, C., Burton-Danner, K., and Jackson, G. R. (2000). Aging and spatial localization during feature search. Gerontology 46, 300-305.
53. Payer, D., Marshuetz, C., Sutton, B., Hebrank, A., Welsh, R. C., and Park, D. C. (2006). Decreased neural specialization in old adults on a working memory task. Neuroreport 17, 487-491.
54. Petkov, C. I., Kang, X., Alho, K., Bertrand, O., Yund, E. W., and Woods, D. L. (2004). Attentional modulation of human auditory cortex. Nat. Neurosci. 7, 658-663.
55. Polich, J., and McIsaac, H. K. (1994). Comparison of auditory P300 habituation from active and passive conditions. Int. J. Psychophysiol. 17, 25-34.
56. Preston, A. R., Thomason, M. E., Ochsner, K. N., Cooper, J. C., and Glover, G. H. (2004). Comparison of spiral-in/out and spiral-out BOLD fMRI at 1.5 and 3 T. Neuroimage 21, 291-301.
57. Riecker, A., Wildgruber, D., Mathiak, K., Grodd, W., and Ackermann, H. (2003). Parametric analysis of rate-dependent hemodynamic response functions of cortical and subcortical brain structures during auditorily cued finger tapping: a fMRI study. Neuroimage 18, 731-739.
58. Ross, B., Fujioka, T., Tremblay, K. L., and Picton, T. W. (2007). Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J. Neurosci. 27, 11172-11178.
59. Sable, J. J., Low, K. A., Maclin, E. L., Fabiani, M., and Gratton, G. (2004). Latent inhibition mediates N1 attenuation to repeating sounds. Psychophysiology 41, 636-642.
60. Sampson, P. D., Streissguth, A. P., Barr, H. M., and Bookstein, F. L. (1989). Neurobehavioral effects of prenatal alcohol: part II. Partial least squares analysis. Neurotoxicol. Teratol. 11, 477-491.
61. Schmidt, S., Redecker, C., Bruehl, C., and Witte, O. W. (2010). Age-related decline of functional inhibition in rat cortex. Neurobiol. Aging 31, 504-511.
62. Schmitz, T. W., Cheng, F. H., and De Rosa, E. (2010). Failing to ignore: paradoxical neural effects of perceptual load on early attentional selection in normal aging. J. Neurosci. 30, 14750-14758.
63. Schmolesky, M. T., Wang, Y., Pu, M., and Leventhal, A. G. (2000). Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys. Nat. Neurosci. 3, 384-390.
64. Shelley, A. M., Ward, P. B., Michie, P. T., Andrews, S., Mitchell, P. F., Catts, S. V., and McConaghy, N. (1991). The effect of repeated testing on ERP components during auditory selective attention. Psychophysiology 28, 496-510.
65. Slotnick, S. D., Thompson, W. L., and Kosslyn, S. M. (2005). Visual mental imagery induces retinotopically organized activation of early visual areas. Cereb. Cortex 15, 1570-1583.
66. Soldan, A., Gazes, Y., Hilton, H. J., and Stern, Y. (2008). Aging does not affect brain patterns of repetition effects associated with perceptual priming of novel objects. J. Cogn. Neurosci. 20, 1762-1776.
67. Sommers, M. S. (1999). Perceptual specificity and implicit auditory priming in older and younger adults. J. Exp. Psychol. Learn. Mem. Cogn. 25, 1236-1255.
68. Steinmann, I., and Gutschalk, A. (2010). Potential fMRI correlates of 40-Hz phase locking in primary auditory cortex, thalamus and midbrain. Neuroimage 54, 495-504.
69. Summerfield, C., Trittschuh, E. H., Monti, J. M., Mesulam, M. M., and Egner, T. (2008). Neural repetition suppression reflects fulfilled perceptual expectations. Nat. Neurosci. 11, 1004-1006.
70. Tian, B., Reser, D., Durham, A., Kustov, A., and Rauschecker, J. P. (2001). Functional specialization in rhesus monkey auditory cortex. Science 292, 290-293.
71. van Turennout, M., Ellmore, T., and Martin, A. (2000). Long-lasting cortical plasticity in the object naming system. Nat. Neurosci. 3, 1329-1334.
72. Wambacq, I. J., Koehnke, J., Besing, J., Romei, L. L., Depierro, A., and Cooper, D. (2009). Processing interaural cues in sound segregation by young and middle-aged brains. J. Am. Acad. Audiol. 20, 453-458.
73. Wiggs, C. L., and Martin, A. (1998). Properties and mechanisms of perceptual priming. Curr. Opin. Neurobiol. 8, 227-233.
74. Wiggs, C. L., Weisberg, J., and Martin, A. (2006). Repetition priming across the adult lifespan - the long and short of it. Neuropsychol. Dev. Cogn. B. Aging Neuropsychol. Cogn. 13, 308-325.
75. Wig, G. S., Grafton, S. T., Demos, K. E., and Kelley, W. M. (2005). Reductions in neural activity underlie behavioral components of repetition priming. Nat. Neurosci. 8, 1228-1233.
76. Winston, J. S., Henson, R. N., Fine- Goulden, M. R., and Dolan, R. J. (2004). FMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J. Neurophysiol. 92, 1830-1839.
77. Zatorre, R. J., Mondor, T. A., and Evans, A. C. (1999). Auditory attention to space and frequency activates similar cerebral systems. Neuroimage 10, 544-554.