Auditory object salience: Human cortical processing of non-biological action sounds and their acoustic signal attributes

Frontiers in Systems Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Lewis, James W ^a,b   Talkington, William J ^a,b   Tallaksen, Katherine C ^a,b   Frum, Chris A ^a,b  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Auditory perception; Entropy; Functional MRI; Motion processing; Natural sound categorization; Signal feature extraction; Spectral structure variation

Indexed keywords

ACOUSTICS; ADULT; ARTICLE; AUDITORY DISCRIMINATION; AUDITORY STIMULATION; BRAIN CORTEX; BRAIN FUNCTION; ENTROPY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING; HEARING ACUITY; HUMAN; HUMAN EXPERIMENT; MALE; NONBIOLOGICAL ACTION SOUNDS; NORMAL HUMAN; SOUND; SOUND RELATED PHENOMENA; SOUND TRANSMISSION; SPECTRAL STRUCTURE VARIATION; SUPERIOR TEMPORAL GYRUS;

EID: 84861859221     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2012.00027     Document Type: Article

References (116)

1. Aglioti, S. M., Cesari, P., Romani, M., and Urgesi, C. (2008). Action anticipation and motor resonance in elite basketball players. Nat. Neurosci. 11, 1109-1116.
2. Allison, T., McCarthy, G., Nobre, A., Puce, A., and Belger, A. (1994). Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. Cereb. Cortex 5, 544-554.
3. Antal, T., Droz, M., Gyorgyi, G., and Racz, Z. (2002). Roughness distributions for 1/f alpha signals. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 65, 046140.
4. Attias, H., and Schreiner, C. E. (1997). Temporal low-order statistics of natural sounds. Adv. Neural Info. Process. Syst. 9, 27-33.
5. Aziz-Zadeh, L., Iacoboni, M., Zaidel, E., Wilson, S., and Mazziotta, J. (2004). Left hemisphere motor facilitation in response to manual action sounds. Eur. J. Neurosci. 19, 2609-2612.
6. Barsalou, L. W. (2008). Grounded cognition. Annu. Rev. Psychol. 59, 617-645.
7. Baumgart, F., Gaschler-Markefski, B., Woldorff, M. G., Heinze, H-J., and Scheich, H. (1999). A movement-sensitive area in auditory cortex. Nature 400, 724-725.
8. Beauchamp, M., Lee, K., Haxby, J., and Martin, A. (2002). Parallel visual motion processing streams for manipulable objects and human movements. Neuron 34, 149-159.
9. Belin, P., Zatorre, R. J., Hoge, R., Evans, A. C., and Pike, B. (1999). Eventrelated fMRI of the auditory cortex. Neuroimage 10, 417-429.
10. Bidet-Caulet, A., Voisin, J., Bertrand, O., and Fonlupt, P. (2005). Listening to a walking human activates the temporal biological motion area. Neuroimage 28, 132-139.
11. Bregman, A. S. (1990). Auditory Scene Analysis. Cambridge, MA: MIT Press.
12. Caramazza, A., and Mahon, B. Z. (2003). The organization of conceptual knowledge: the evidence from category-specific semantic deficits. Trends Cogn. Sci. 7, 354-361.
13. Cavanagh, P. (1992). Attention-based motion perception. Science 257, 1563-1565.
14. Chao, L. L., and Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478-484.
15. Chubb, C., and Sperling, G. (1988). Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. J. Opt. Soc. Am. A 5, 1986-2007.
16. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173.
17. Cronbach, L. J. (1951). Coefficient alpha and the internal structure of tests. Psychometrika 16, 297-334.
18. Cusack, R. (2005). The intraparietal sulcus and perceptual organization. J. Cogn. Neurosci. 17, 641-651.
19. Cusack, R., and Carlyon, R. P. (2003). Perceptual asymmetries in audition. J. Exp. Psychol. Hum. Percept. Perform. 29, 713-725.
20. de Lucia, M., Camen, C., Clarke, S., and Murray, M. M. (2009). The role of actions in auditory object discrimination. Neuroimage 48, 475-485.
21. Doniger, G. M., Foxe, J. J., Murray, M. M., Higgins, B. A., Snodgrass, J. G., Schroeder, C. E., and Javitt, D. C. (2000). Activation timecourse of ventral visual stream object-recognition areas: high density electrical mapping of perceptual closure processes. J. Cogn. Neurosci. 12, 615-621.
22. Downing, P. E., Jiang, Y., Shuman, M., and Kanwisher, N. (2001). A cortical area selective for visual processing of the human body. Science 293, 2470-2473.
23. Dykstra, A. R., Halgren, E., Thesen, T., Carlson, C. E., Doyle, W., Madsen, J. R., Eskandar, E. N., and Cash, S. S. (2011). Widespread brain areas engaged during a classical auditory streaming task revealed by intracranial EEG. Front. Hum. Neurosci. 5:74. doi: 10.3389/fnhum.2011.00074
24. Edmister, W. B., Talavage, T. M., Ledden, P. J., and Weisskoff, R. M. (1999). Improved auditory cortex imaging using clustered volume acquisitions. Hum. Brain Mapp. 7, 89-97.
25. Elhilali, M., and Shamma, S. A. (2008). A cocktail party with a cortical twist: how cortical mechanisms contribute to sound segregation. J. Acoust. Soc. Am. 124, 3751-3771.
26. Engel, L. R., Frum, C., Puce, A., Walker, N. A., and Lewis, J. W. (2009). Different categories of living and non-living sound-sources activate distinct cortical networks. Neuroimage 47, 1778-1791.
27. Epstein, R., and Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature 392, 598-601.
28. Epstein, R. A., Higgins, J. S., Jablonski, K., and Feiler, A. M. (2007). Visual scene processing in familiar and unfamiliar environments. J. Neurophysiol. 97, 3670-3683.
29. Epstein, R. A., and Morgan, L. K. (2011). Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis. Neuropsychologia 50, 530-543.
30. Felleman, D. J., and van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1-47.
31. Fransson, P., and Marrelec, G. (2008). The precuneus/posterior cingulated cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 42, 1178-1184.
32. Frith, C. D., and Frith, U. (1999). Interacting minds-a biological basis. Science 286, 1692-1695.
33. Fritz, J. B., Elhilali, M., and Shamma, S. A. (2007a). Adaptive changes in cortical receptive fields induced by attention to complex sounds. J. Neurophysiol. 98, 2337-2346.
34. Fritz, J. B., Elhilali, M., David, S. V., and Shamma, S. A. (2007b). Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? Hear. Res. 229, 186-203.
35. Gazzola, V., Aziz-Zadeh, L., and Keysers, C. (2006). Empathy and the somatotopic auditory mirror system in humans. Curr. Biol. 16, 1824-1829.
36. Glover, G. H., and Law, C. S. (2001). Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn. Reson. Med. 46, 515-522.
37. Goll, J. C., Crutch, S. J., and Warren, J. D. (2011). Central auditory disorders: toward a neuropsychology of auditory objects. Curr. Opin. Neurol. 23, 617-627.
38. Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253-258.
39. Griffiths, T. D., Bench, C. J., and Frackowiak, R. S. J. (1994). Human cortical areas selectively activated by apparent sound movement. Curr. Biol. 4, 892-895.
40. Griffiths, T. D., Kumar, S., Warren, J. D., Stewart, L., Stephan, K. E., and Friston, K. J. (2007). Approaches to the cortical analysis of auditory objects. Hear. Res. 229, 46-53.
41. Griffiths, T. D., and Warren, J. D. (2002). The planum temporale as a computational hub. Trends Neurosci. 25, 348-353.
42. Griffiths, T. D., and Warren, J. D. (2004). What is an auditory object? Nat. Rev. Neurosci. 5, 887-892.
43. 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.
44. Grill-Spector, K., Kushnir, T., Hendler, T., Edelman, S., Itzchak, Y., and Malach, R. (1998). A sequence of object-processing stages revealed by fMRI in the human occipital lobe. Hum. Brain Mapp. 6, 316-328.
45. Gron, G., Wunderlich, A. P., Spitzer, M., Tomczak, R., and Riepe, M. W. (2000). Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat. Neurosci. 3, 404-408.
46. Gygi, B., Kidd, G. R., and Watson, C. S. (2004). Spectral-temporal factors in the identification of environmental sounds. J. Acoust. Soc. Am. 115, 1252-1265.
47. Hall, D. A., Haggard, M. P., Akeroyd, M. A., Palmer, A. R., Summerfield, A. Q., Elliott, M. R., Gurney, E. M., and Bowtell, R. W. (1999). "Sparse" temporal sampling in auditory fMRI. Hum. Brain Mapp. 7, 213-223.
48. Hassabis, D., Kumaran, D., and Maguire, E. A. (2007). Using imagination to understand the neural basis of episodic memory. J. Neurosci. 27, 14365-14374.
49. Hasson, U., Harel, M., Levy, I., and Malach, R. (2003). Large-scale mirror-symmetry organization of human occipitotemporal object areas. Neuron 37, 1027-1041.
50. Howard, M. A., Volkov, I. O., Mirsky, R., Garell, P. C., Noh, M. D., Granner, M., Damasio, H., Stein-schneider, M., Reale, R. A., Hind, J. E., and Brugge, J. F. (2000). Auditory cortex on the human posterior superior temporal gyrus. J. Comp. Neurol. 416, 79-92.
51. Huddleston, W. E., Lewis, J. W., Phinney, R. E. Jr., and de Yoe, E. A. (2008). Auditory and visual attention-based apparent motion share functional parallels. Percept. Psychophys. 70, 1207-1216.
52. Hughes, H. C., Darcey, T. M., Barkan, H. I., Williamson, P. D., Roberts, D. W., and Aslin, C. H. (2001). Responses of human auditory association cortex to the omission of an expected acoustic event. Neuroimage 13, 1073-1089.
53. Husain, F. T., Tagamets, M. A., Fromm, S. J., Braun, A. R., and Horwitz, B. (2004). Relating neuronal dynamics for auditory object processing to neuroimaging activity: a computational modeling and an fMRI study. Neuroimage 21, 1701-1720.
54. Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J. C., and Rizzolatti, G. (2005). Grasping the intentions of others with one's own mirror neuron system. PLoS Biol. 3:e79. 529-535. doi: 10.1371/journal.pbio.0030079
55. Johansson, G. (1973). Visual perceptionof biological motion and a model for its analysis. Percept. Psychophys. 14, 201-211.
56. Julesz, B. (1980). Spatial nonlinearities in the instantaneous perception of textures with identical power spectra. Philos. Trans. R. Soc. Lond. B Biol. Sci. 290, 83-94.
57. Kaas, J. H., and Hackett, T. A. (1998). Subdivisions of auditory cortex and levels of processing in primates. Audiol. Neurootol. 3, 73-85.
58. Kaas, J. H., Hackett, T. A., and Tramo, M. J. (1999). Auditory processing in primate cerebral cortex. Curr. Opin. Neurobiol. 9, 164-170.
59. Kanwisher, N., Chun, M. M., McDermott, J., and Ledden, P. J. (1996). Functional imaging of human visual recognition. Brain Res. Cogn. Brain Res. 5, 55-67.
60. Kanwisher, N., McDermott, J., and Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302-4311.
61. King, A. J., and Nelken, I. (2009). Unraveling the principles of auditory cortical processing: can we learn from the visual system? Nat. Neurosci. 12, 698-701.
62. Kohler, E., Keysers, C., Umilta, A., Fogassi, L., Gallese, V., and Rizzolatti, G. (2002). Hearing sounds, understanding actions: action representation in mirror neurons. Science 297, 846-848.
63. Kourtzi, Z., and Kanwisher, N. (2000). Cortical regions involved in perceiving object shape. J. Neurosci. 20, 3310-3318.
64. Kumar, S., Stephan, K. E., Warren, J. D., Friston, K. J., and Griffiths, T. D. (2007). Hierarchical processing of auditory objects in humans. PLoS Comput. Biol. 3:e100. doi: 10.1371/journal.pcbi.0030100
65. Laaksonen, J. T., Markus Koskela, J., and Oja, E. (2004). Class distributions on SOM surfaces for feature extraction and object retrieval. Neural Netw. 17, 1121-1133.
66. Leaver, A. M., and Rauschecker, J. P. (2010). Cortical representation of natural complex sounds: effects of acoustic features and auditory object category. J. Neurosci. 30, 7604-7612.
67. Leech, R., Holt, L. L., Devlin, J. T., and Dick, F. (2009). Expertise with artificial nonspeech sounds recruits speech-sensitive cortical regions. J. Neurosci. 29, 5234-5239.
68. Lewis, J. W. (2010). "Audio-visual perception of everyday natural objects-hemodynamic studies in humans," in Multisensory Object Perception in the Primate Brain, eds J. Marcusand and P. J. K. Naumer, (Springer Science+Business Media, LLC), 155-190.
69. Lewis, J. W., Beauchamp, M. S., and de Yoe, E. A. (2000). A comparison of visual and auditory motion processing in human cerebral cortex. Cereb. Cortex 10, 873-888.
70. Lewis, J. W., Phinney, R. E., Brefczynski-Lewis, J. A., and de Yoe, E. A. (2006). Lefties get it "right" when hearing tool sounds. J. Cogn. Neurosci. 18, 1314-1330.
71. Lewis, J. W., Talkington, W. J., Puce, A., Engel, L. R., and Frum, C. (2011). Cortical networks representing object categories and high-level attributes of familiar real-world action sounds. J. Cogn. Neurosci. 23, 2079-2101.
72. Lewis, J. W., Talkington, W. J., Walker, N. A., Spirou, G. A., Jajosky, A., Frum, C., and Brefczynski-Lewis, J. A. (2009). Human cortical organization for processing vocalizations indicates representation of harmonic structure as a signal attribute. J. Neurosci. 29, 2283-2296.
73. Lewis, J. W., Wightman, F. L., Brefczynski, J. A., Phinney, R. E., Binder, J. R., and de Yoe, E. A. (2004). Human brain regions involved in recognizing environ-mental sounds. Cereb. Cortex 14, 1008-1021.
74. Macevoy, S. P., and Epstein, R. A. (2011). Constructing scenes from objects in human occipitotemporal cortex. Nat. Neurosci. 14, 1323-1329.
75. 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.
76. Mäkelä, J. P., and McEvoy, L. (1996). Auditory evoked fields to illusory sound source movements. Exp. Brain Res. 110, 446-453.
77. Malach, R., Reppas, J. B., Benson, R. R., Kwong, K. K., Jiang, H., Kennedy, W. A., Ledden, P. J., Brady, T. J., Rosen, B. R., and Tootell, R. B. H. (1995). Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl. Acad. Sci. U.S.A. 92, 8135-8139.
78. Martin, A. (2007). The representation of object concepts in the brain. Annu. Rev. Psychol. 58, 25-45.
79. McCarthy, G., Puce, A., Gore, J. C., and Allison, T. (1997). Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605-610.
80. McDermott, J. H., and Oxenham, A. J. (2008). Spectral completion of partially masked sounds. Proc. Natl. Acad. Sci. U.S.A. 105, 5939-5944.
81. McDermott, J. H., and Simoncelli, E. P. (2011). Sound texture perception via statistics of the auditory periphery: evidence from sound synthesis. Neuron 71, 926-940.
82. Medvedev, A. V., Chiao, F., and Kanwal, J. S. (2002). Modeling complex tone perception: grouping harmonics with combination-sensitive neurons. Biol. Cybern. 86, 497-505.
83. Minda, J. P., and Ross, B. H. (2004). Learning categories by making pre-dictions: an investigation of indirect category learning. Mem. Cognit. 32, 1355-1368.
84. Mormann, F., Dubois, J., Kornblith, S., Milosavljevic, M., Cerf, M., Ison, M., Tsuchiya, N., Kraskov, A., Quiroga, R. Q., Adolphs, R., Fried, I., and Koch, C. (2011). A category-specific response to animals in the right human amygdala. Nat. Neurosci. 14, 1247-1249.
85. Morosan, P., Rademacher, J., Schleicher, A., Amunts, K., Schormann, T., and Zilles, K. (2001). Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13, 684-701.
86. Murray, S. O., Newman, A. J., Roder, B., Mitchell, T. V., Takahashi, T., and Neville, H. J. (1998). Functional organization of auditory motion processing in humans using fMRI. Soc. Neurosci. Abstr. 24, 1401.
87. Nelken, I. (2004). Processing of complex stimuli and natural scenes in the auditory cortex. Curr. Opin. Neurobiol. 14, 474-480.
88. Nunnally, J. C. (1978). Psychometric Theory. New York, NY: McGraw-Hill.
89. Obleser, J., Eisner, F., and Kotz, S. A. (2008). Bilateral speech comprehension reflects differential sensitivity to spectral and temporal features. J. Neurosci. 28, 8116-8123.
90. Obleser, J., Zimmermann, J., van Meter, J., and Rauschecker, J. P. (2007). Multiple stages of auditory speech perception reflected in event-related FMRI. Cereb. Cortex 17, 2251-2257.
91. Overath, T., Kumar, S., Stewart, L., von Kriegstein, K., Cusack, R., Rees, A., and Griffiths, T. D. (2010). Cortical mechanisms for the segregation and representation of acoustic textures. J. Neurosci. 30, 2070-2076.
92. Pelphrey, K. A., Morris, J. P., and McCarthy, G. (2004). Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. J. Cogn. Neurosci. 16, 1706-1716.
93. Rademacher, J., Morosan, P., Schormann, T., Schleicher, A., Werner, C., Freund, H. J., and Zilles, K. (2001). Probabilistic mapping and volume measurement of human primary auditory cortex. Neuroimage 13, 669-683.
94. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
95. Rauschecker, J. P., and Scott, S. K. (2009). Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat. Neurosci. 12, 718-724.
96. Rauschecker, J. P., Tian, B., and Hauser, M. (1995). Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268, 111-114.
97. Reddy, R. K., Ramachandra, V., Kumar, N., and Singh, N. C. (2009). Categorization of environmental sounds. Biol. Cybern. 100, 299-306.
98. Rizzolatti, G., and Craighero, L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169-192.
99. Rizzolatti, G., Luppino, G., and Matelli, M. (1998). The organization of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol. 106, 283-296.
100. Rosch, E. H. (1973). Natural categories. Cogn. Psychol. 4, 328-350.
101. Rutishauser, U., Tudusciuc, O., Neumann, D., Mamelak, A. N., Heller, A. C., Ross, I. B., Philpott, L., Sutherling, W. W., and Adolphs, R. (2011). Single-unit responses selective for whole faces in the human amygdala. Curr. Biol. 21, 1654-1660.
102. Sathian, K., Lacey, S., Stilla, R., Gibson, G. O., Deshpande, G., Hu, X., Laconte, S., and Glielmi, C. (2011). Dual pathways for haptic and visual perception of spatial and texture information. Neuroimage 57, 462-475.
103. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. New York, NY: Thieme Medical Publishers.
104. Talkington, W. J., Rapuano, K. M., Hitt, L., Frum, C. A., and Lewis, J. W. (in press) Humans mimicking animals: a cortical hierarchy for human vocal communication sounds. J. Neurosci.
105. Tchernichovski, O., Mitra, P. P., Lints, T., and Nottebohm, F. (2001). Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291, 2564-2569.
106. Teki, S., Chait, M., Kumar, S., von Kriegstein, K., and Griffiths, T. D. (2011). Brain bases for auditory stimulus-driven figure-ground segregation. J. Neurosci. 31, 164-171.
107. Tootell, R. B., Mendola, J. D., Hadjikhani, N. K., Liu, A. K. and Dale, A. M. (1998). The representation of the ipsilateral visual field in human cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 95, 818-824.
108. van Essen, D. C. (2005). A Population-Average, Landmark-and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28, 635-662.
109. van Essen, D. C., Drury, H. A., Dickson, J., Harwell, J., Hanlon, D., and Anderson, C. H. (2001). An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 8, 443-459.
110. Vogt, B. A., Finch, D. M., and Olson, C. R. (1992). Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex 2, 435-443.
111. Voss, R. F., and Clarke, J. (1975). 1/f noise in music and speech. Nature 258, 317-318.
112. Warren, J., Zielinski, B., Green, G., Rauschecker, J., and Griffiths, T. (2002). Perception of sound-source motion by the human brain. Neuron 34, 139-148.
113. Warren, R. M., Obusek, C. J., and Ackroff, J. M. (1972). Auditory induction: perceptual synthesis of absent sounds. Science 176, 1149-1151.
114. Woods, D. L., Herron, T. J., Cate, A. D., Yund, E. W., Stecker, G. C., Rinne, T., and Kang, X. (2010). Functional properties of human auditory cortical fields. Front. Syst. Neurosci. 4:155. doi: 10.3389/fnsys.2010.00155
115. Zatorre, R. J., Bouffard, M., and Belin, P. (2004). Sensitivity to auditory object features in human temporal neocortex. J. Neurosci. 24, 3637-3642.
116. Zatorre, R. J., Evans, A. C., Meyer, E., and Gjedde, A. (1992). Lateralization of phonetic and pitch discrimination in speech processing. Science 256, 846-849.