Sound-induced flash illusion in older adults: Evidence from low-frequency fluctuation amplitudes in resting-state fMRI

doi:10.3724/SP.J.1041.2020.00823

Abstract

Abstract:

Auditory dominance means that the auditory information in multisensory integration is given priority and processed in a dominant position. Sound-induced flash illusion (SiFI) is a typical auditory dominance phenomenon, in which the visual perception of a stimulus for briefly heard voices, qualitatively changing at the same time, results in a fission illusion (F1B2) and a fusion illusion (F2B1). Previous studies have shown that older adults experience illusions more often than young adults. However, there is not yet a consensus regarding the mechanism when it is investigated using resting-state fMRI, though resting-state neural activity can reveal the intrinsic functional architecture of the brain (Fox & Raichle, 2007). Therefore, the present study aimed to investigate how amplitude of low-frequency ?uctuations (ALFF) was related to SiFI in older adults and would provide important novel insights into the differences in SiFI between older and young adults.

We selected 50 older adults (ages: 50~69 year old, M = 61.78, SD = 4.17) and 50 young adults (ages: 17~27 year old, M = 20.86, SD = 2.17). The present study was a 2 (participants: older vs. young adults) × 2 (flash number: 1 vs. 2) × 3 (sound number: 0 vs. 1 vs 2) mixed design. RS-fMRI data were collected by a magnetic resonance scanner in the participants’ natural state of wakefulness and relaxation. The RS-fMRI data were obtained by a Philips 3.0T magnetic resonance scanner, and the images of all participants’ resting states were obtained by gradient echoplanar imaging (EPI). The scan parameters were as follows: the TR = 2000 ms, TE = 30 ms, of view (FOV) = 220 mm × 220 mm, Turn corner = 90°, matrix = 64×64, Layer number = 36, layer thickness = 4 mm, with a thick layer of scanning time 400 s. We used the ALFF of the resting state of the brain to investigate the correlation between SiFI and spontaneous brain region activity in older and young adults to reveal SiFI differences. ALFF results were calculated using DPABI, a RS-fMRI data processing software (Yan et al., 2016).

From the perspective of the accuracy results, older and young adults both experienced fission and fusion illusions. However, regardless of experiencing a fission illusion or a fusion illusion, the size of illusion experienced by older adults was greater than that experienced by young adults. From the correlation analysis results of ALFF and illusions, there was a significant positive correlation between the F1B2 illusion and spontaneous medial prefrontal cortex (MPFC) activity in older adults, and there was a significant negative correlation between the F1B2 illusion and spontaneous activity in the right superior occipital gyrus (SOG) and the left lingual gyrus in young adults. For the F2B1 illusion, there was a significant negative correlation between the F2B1 illusion and spontaneous activity in the right superior occipital gyrus (SOG), the left lingual gyrus (IFG) and the right cerebellum, and a significant positive correlation between the F2B1 illusion and spontaneous activity in the left inferior frontal gyrus (IFG), the right middle frontal gyrus (MFG) and the left inferior temporal gyrus (ITG) in older adults. However, there was a significant positive correlation between the F2B1 illusion and spontaneous activity in the left superior frontal gyrus (SFG) in young adults.

The present study showed that the increased illusion experienced by older adults was related to spontaneous activity during resting states in multiple brain regions.

Key words: sound-induced flash illusion (SiFI), resting-state functional magnetic resonance imaging (RS-fMRI), amplitude of low-frequency ?uctuations (ALFF), fission illusion, fusion illusion

ZHOU Heng, HE Hua, YU Wei, WANG Aijun, ZHANG Ming. (2020). Sound-induced flash illusion in older adults: Evidence from low-frequency fluctuation amplitudes in resting-state fMRI. Acta Psychologica Sinica, 52(7), 823-834.

Figures/Tables 4

Figure 1. A schematic of a behavioral experiment

Figure 2. The average correct rate of the old and the young under each experimental condition (%)
Note. *p < 0.05, ***p < 0.001

Figure 3. Top (A) ALFF was significantly correlated with mean ALFF on F1B2, and Top (B) scatter plot was significantly correlated with mean ALFF on Prefrontal_Med_L (r = 0.55, p < 0.001). Bottom (A) F1B2 condition, ALFF was significantly correlated with the size of illusion, and Bottom (B) scatter plot was significantly correlated with mean ALFF on Occipital_Sup_R (r = -0.45, p = 0.001). (Color bars represent R-values, L = Left, R = right. MNI = Montreal Neurological Institute.)

Figure 4. Top (A) ALFF was significantly correlated with mean ALFF in F2B1, and Top (B) scatter plot was significantly correlated with mean ALFF in Frontal (r = 0.40, p = 0.004). Bottom (A) F2B1 condition, ALFF was significantly correlated with mean ALFF, and Bottom (B) scatter plot was significantly correlated with mean ALFF on Frontal (r = 0.55, p < 0.001). (Color bars represent R-values, L = Left, R = right. MNI = Montreal Neurological Institute.)

References 67

1	Andersen, T. S., Tiippana, K., & Sams, M . ( 2004). Factors influencing audiovisual fission and fusion illusions. Cognitive Brain Research, 21( 3), 301-308. doi: 10.1016/j.cogbrainres.2004.06.004 URL pmid: 15511646
2	Baddeley, A., DellaSala, S., Papagno, C., & Spinnler, H . ( 1997). Dual-task performance in dysexecutive and nondysexecutive patients with a frontal lesion. Neuropsychology, 11( 2), 187-194. doi: 10.1037//0894-4105.11.2.187 URL pmid: 9110326
3	Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S . ( 1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34( 4), 537-541.
4	Bolognini, N., Rossetti, A., Casati, C., Mancini, F., & Vallar, G . ( 2011). Neuromodulation of multisensory perception: A tdcs study of the sound-induced flash illusion. Neuropsychologia, 49( 2), 231-237. doi: 10.1016/j.neuropsychologia.2010.11.015 URL pmid: 21094177
5	Cecere, R., Rees, G., & Romei, V . ( 2015). Individual differences in alpha frequency drive crossmodal illusory perception. Current Biology, 25( 2), 231-235. URL pmid: 25544613
6	Chan, J. S., Connolly, S. K., & Setti, A . ( 2018). The number of stimulus-onset asynchronies affects the perception of the sound-induced flash illusion in young and older adults. Multisensroy Research, 31( 3-4), 175-190.
7	Chan, J. S., Kaiser, J., Brandl, M., Matura, S., Prvulovic, D., Hogan, M. J., & Naumer, M. J . ( 2015). Expanded temporal binding windows in people with mild cognitive impairment, Current Alzheimer Research, 12( 1), 61-68. doi: 10.2174/1567205012666141218124744 URL pmid: 25523426
8	Chen, Q., & Zhou, X. L. ( 2013). Vision dominates at the preresponse level and audition dominates at the response level in cross-modal interaction: Behavioral and neural evidence. Journal of Neuroscience, 33( 17), 7109-7121. URL pmid: 23616521
9	de Haas, B., Kanai, R., Jalkanen, L., & Rees, G . ( 2012). Grey matter volume in early human visual cortex predicts proneness to the sound-induced flash illusion. Proceedings of the Royal Society B-Biological Sciences, 279( 1749), 4955-4961.
10	DeLoss, D. J., Pierce, R. S., & Andersen, G. J . ( 2013). Multisensory integration, aging, and the sound-induced flash illusion. Psychology and Aging, 28( 3), 802-812.
11	Diaconescu, A. O., Hasher, L., & Mcintosh, A. R . ( 2013). Visual dominance and multisensory integration changes with age. Neuroimage, 65( 1), 152-166.
12	Diederich, A., Colonius, H., & Schomburg, A . ( 2008). Assessing age-related multisensory enhancement with the time-window- of-integration model. Neuropsychologia, 46( 10), 2556-2562. URL pmid: 18490033
13	Driver, J., & Noesselt, T. ( 2008). Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments. Neuron, 57( 1), 11-23.
14	Falchier, A., Clavagnier, S., Barone, P., & Kennedy, H . ( 2002). Anatomical evidence of multimodal integration in primate striate cortex. Journal of Neuroscience, 22( 13), 5749-5759.
15	Freiherr, J., Lundström, J. N., Habel, U., & Reetz, K . ( 2013). Multisensory integration mechanisms during aging. Frontiers in Human Neuroscience, 7( 7), 863.
16	Gilbert, S. J., & Burgess, P. W. ( 2008). Executive function. Current Biology, 18( 3), R110-R114. URL pmid: 18269902
17	Hirst, R. J., Setti, A., Kenny, R. A., & Newell, F. N . ( 2019). Age-related sensory decline mediates the sound-induced flash illusion: Evidence for reliability weighting models of multisensory perception. Scientific Reports, 9, 19347.
18	He, Y., Wang, L., Zang, Y., Tian, L., Jiang, T., Li, K., & Jiang, T . ( 2007). Regional coherence changes in the early stages of Alzheimer’s disease: A combined structural and resting- state functional MRI study. NeuroImage, 35( 2), 488-500.
19	Innes-Brown, H., & Crewther, D. ( 2009). The impact of spatial incongruence on an auditory-visual illusion. PLoS ONE, 4( 7), e6450. doi: 10.1371/journal.pone.0006450 URL pmid: 19649293
20	Kamke, M. R., Vieth, H. E., Cottrell, D., & Mattingley, J. B . ( 2012). Parietal disruption alters audiovisual binding in the sound-induced flash illusion. NeuroImage, 62( 3), 1334-1341. doi: 10.1016/j.neuroimage.2012.05.063 URL pmid: 22658974
21	Kaposvari, P., Bognar, A., Csibri, P., Utassy, G., & Sary, G . ( 2014). Fusion and fission in the visual pathways. Physiological Research, 63( 5), 625-635. URL pmid: 24908093
22	Kawachi, J. ( 2017). Brodmann areas 17, 18, and 19 in the human brain: An overview. Brain and Nerve, 69( 4), 397-410.
23	Keil, J., Nadia, M., Hartmann, T., & Weisz, N . ( 2013). Prestimulus beta power and phase synchrony influence the sound-induced flash illusion. Cerebral cortex, 24( 5), 1278-1288. doi: 10.1093/cercor/bhs409 URL pmid: 23300109
24	Klatzky, R. L., Marston, J. R., Giudice, N. A., Golledge, R. G., & Loomis, J. M . ( 2006). Cognitive load of navigating without vision when guided by virtual sound versus spatial language. Journal Experimental Psychology: Applied, 12( 4), 223-232.
25	Koelewijn, T., Bronkhorst, A., & Theeuwes, J . ( 2010). Attention and the multiple stages of multisensory integration: A review of audiovisual studies. Acta Psychologica, 134( 3), 372-384.
26	Jiang, Y., & Han, S. H. ( 2007). Perceptual gain and perceptual loss: Distinct neural mechanisms of audiovisual interactions. International Journal of Magnetic Resonance Imaging, 1( 1), 1749-8023.
27	Laurienti, P. J., Burdette, J. H., Maldjian, J. A., & Wallace, M. T . ( 2006). Enhanced multisensory integration in older adults. Neurobiology of Aging, 27( 8), 1155-1163. URL pmid: 16039016
28	Lei, X. X., Zhong, M. T., Liu, Y., Jin, X. H., Zhou, Q., Xi, C., .. Yi, J. Y . ( 2017). A resting-state fMRI study in borderline personality disorder combining amplitude of low frequency fluctuation, regional homogeneity and seed based functional connectivity. Journal of Affective Disorders, 218, 299-305. URL pmid: 28478359
29	Li, C. M., Liu, C., Yin, X. T., Yang, J., Gui, L., Wei, L. Q., Wang, J . ( 2014). Frequency-dependent changes in the amplitude of low-frequency fluctuations in subcortical ischemic vascular disease (SIVD): A resting-state fMRI study. Behavioural Brain Research, 274, 205-210. doi: 10.1016/j.bbr.2014.08.019 URL pmid: 25138697
30	Li, Y., & Shu, H. ( 2014). The brain mechanisms and functional hypothesis of default mode network and its clinical application. Advances in Psychological Science, 22(2), 234-249.
31	Luo, Y. M., Li, B. L., Liu, J., Bi, Z. Z., & Huang, X. T . ( 2015). Amplitude of low-frequency fluctuations in happiness: A resting-state fMRI study. Chinese Science Bulletin, 60( 2), 170-178.
32	Maccora, S., Giglia, G., Bolognini, N., Cosentino, G., Gangitano, M., Salemi, G., & Brighina, F . ( 2019). Cathodal occipital tDCS is unable to modulate the sound induced flash illusion in migraine. Frontiers in Human Neuroscience, 13, 247. doi: 10.3389/fnhum.2019.00247 URL pmid: 31379542
33	Mahoney, J. R., Li, P. C. C., Ohpark, M., Verghese, J., & Holtzer, R . ( 2011). Multisensory integration across the senses in young and old adults. Brain Research, 1426( 17), 43-53.
34	Mcdowell, S., Whyte, J., & D'Esposito, M . ( 1997). Working memory impairments in traumatic brain injury: evidence from a dual-task paradigm. Neuropsychologia, 35( 10), 1341-1353. doi: 10.1016/s0028-3932(97)00082-1 URL pmid: 9347480
35	Mcgovern, D. P., Eugenie, R., John, S., Martin, M. G. T., & Newell, F. N . ( 2014). The sound-induced flash illusion reveals dissociable age-related effects in multisensory integration. Frontiers in Aging Neuroscience, 6, 250. URL pmid: 25309430
36	Mennes, M., Zuo, X. N., Kelly, C., Martino, A. D., Zang, Y. F., Biswal, B., .. Milham M., P . ( 2011). Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics. NeuroImage, 54( 4), 2950-2959.
37	Merriman, N. A., Whyatt, C., Setti, A., Craig, C., & Newell, F. N . ( 2015). Successful balance training is associated with improved multisensory function in fall-prone older adults. Computers in Human Behavior, 45, 192-203.
38	Mishra, J., Martinez, A., & Hillyard, S. A . ( 2009). Effect of attention on early cortical processes associated with the sound-induced extra flash illusion. Journal of Cognitive Neuroscience, 22( 8), 1714-1729.
39	Mishra, J., Martinez, A., Sejnowski, T. J., & Hillyard, S. A . ( 2007). Early cross-modal interactions in auditory and visual cortex underlie a sound-induced visual illusion. Journal of Neuroscience, 27( 15), 4120-4131. URL pmid: 17428990
40	Pan, W., Wang, T., Wang, X., Hitchman, G., Wang, L., & Chen, A . ( 2014). Identifying the core components of emotional intelligence: evidence from amplitude of low-frequency fluctuations during resting state. PloS One, 9( 10), e111435. doi: 10.1371/journal.pone.0111435 URL pmid: 25356830
41	Pan, W. G., Liu, C. C., Yang, Q., Gu, Y., Yin, S. H., & Chen, A. T . ( 2016). The neural basis of trait self-esteem revealed by the amplitude of low-frequency fluctuations and resting state functional connectivity. Social Cognitive and Affective Neuroscience, 11( 3), 367-376.
42	Peiffer, A. M., Mozolic, J. L., Hugenschmidt, C. E., & Laurienti, P. J . ( 2007). Age-related multisensory enhancement in a simple audiovisual detection task. Neuroreport, 18( 10), 1077-1081. doi: 10.1097/WNR.0b013e3281e72ae7 URL pmid: 17558300
43	Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L . ( 2001). A default mode of brain fuction. Proceeding of the National Academy of Sciences of the United States of American, 98( 2), 676-682.
44	Schmitz, T. W., Cheng, F. H. T., & de Rosa, E . ( 2010). Failing to ignore: paradoxical neural effects of perceptual load on early attentional selection in normal aging. Journal of Neuroscience, 30( 44), 14750-14758.
45	Setti, A., Burke, K. E., Kenny, R. A., & Newell, F. N . ( 2011). Is inefficient multisensory processing associated with falls in older adults?. Experimental Brain Research, 209( 3), 375-384. doi: 10.1007/s00221-011-2560-z URL pmid: 21293851
46	Shams, L., Kamitani, Y., & Shimojo, S . ( 2000). Illusions: What you see is what you hear. Nature, 408( 6814), 788-788. doi: 10.1038/35048669 URL pmid: 11130706
47	Shams, L., Kamitani, Y., & Shimojo, S . ( 2002). Visual illusion induced by sound. Cognitive Brain Research, 14( 1), 147-152. doi: 10.1016/s0926-6410(02)00069-1 URL pmid: 12063138
48	Shams, L., & Kim, R. ( 2010). Crossmodal influences on visual perception. Physics of Life Reviews, 7( 3), 269-284. URL pmid: 20447880
49	Shams, L., Ma, W. J., & Beierholm, U . ( 2005). Sound-induced flash illusion as an optimal percept. Neuroreport, 16( 17), 1923-1927. doi: 10.1097/01.wnr.0000187634.68504.bb URL pmid: 16272880
50	Spence, C. ( 2011). Crossmodal correspondences: A tutorial review. Attention, Perception & Psychophysics, 73( 4), 971-995.
51	Stapleton, J., Setti, A., Doheny, E. P., Kenny, R. A., & Newell, F. N . ( 2014). A standing posture is associated with increased susceptibility to the sound-induced flash illusion in fall- prone older adults. Experimental Brain Research, 232( 2), 423-434. doi: 10.1007/s00221-013-3750-7 URL pmid: 24186198
52	Szameitat, A., Schubert, T., Müller, K., & Von Cramon, D . ( 2002). Localization of executive functions in dual-task performance with fMRI. Journal of Cognitive Neuroscience, 14( 8), 1184-1199. URL pmid: 12495525
53	Talsma, D. ( 2015). Predictive coding and multisensory integration: An attentional account of the multisensory mind. Frontiers in Integrative Neuroscience, 9(19), 19-32.
54	Tan, J. F., Wu, S. S., Xu, L., Wang, L. J., & Chen, A. T . ( 2013). Prefrontal cortex with executive functions involved in dual-task performance. Advances in Psychological Science, 21( 12), 2127-2135.
55	Watkins, S., Shams, L., Josephs, O., & Rees, G . ( 2007). Activity in human V1 follows multisensory perception. NeuroImage, 37( 2), 572-578. doi: 10.1016/j.neuroimage.2007.05.027 URL
56	Watkins, S., Shams, L., Tanaka, S., Haynes, J. D., & Rees, G . ( 2006). Sound alters activity in human V1 in association with illusory visual perception. NeuroImage, 31( 3), 1247-1256. doi: 10.1016/j.neuroimage.2006.01.016 URL pmid: 16556505
57	Wang, L. J., Chen, J. T., Yang, Z. Y., Liu, C. C., Deng, Z., & Chen, A. T . ( 2016). Individual differences in the attentional blink: Evidence from the Amplitude of low-frequency fluctuations in non-blinkers and blinkers. Biological Psychology, 114, 33-38. doi: 10.1016/j.biopsycho.2015.11.009 URL pmid: 26610651
58	Wen, Z. L., Fan, X. T., Ye, B. J., & Chen, Y. S . ( 2016). Characteristics of an effect size and appropriateness of mediation effect size measures revisited. Acta Psychologica Sinica, 48( 4), 435-443. doi: 10.3724/SP.J.1041.2016.00435 URL
59	Wozny, D. R., Beierholm, U. R., & Shams, L . ( 2008). Human trimodal perception follows optimal statistical inference. Journal of Vision, 8( 3), 1-11. doi: 10.1167/8.3.14 URL pmid: 18484820
60	Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F . ( 2016). DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics, 14( 3), 339-351. URL pmid: 27075850
61	Yu, W., Wang, A. J., & Zhang, M . ( 2017). Effect of selective and divided attentions on auditory dominance in multisensory integration. Acta Psychologica Sinica, 49( 2), 164-173.
62	Zang, Y., He, Y., Zhu, C., Cao, Q., Sui, M., Liang, M., .. Wang, Y. F . ( 2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain and Development, 29( 2), 83-91. doi: 10.1016/j.braindev.2006.07.002 URL pmid: 16919409
63	Zhang, M., Tang, X. Y., Yu, W., Ning, B., Wang, Z. N., & Wang, A. J . ( 2018). The effects of modal-based endogenous attention on sound-induced flash illusion. Acta Psychologica Sinica, 50( 11), 1212-1221
64	Zhang, N., & Chen, W. ( 2006). A dynamic fmri study of illusory double-flash effect on human visual cortex. Experimental Brain Research, 172( 1), 57-66. doi: 10.1007/s00221-005-0304-7 URL pmid: 16369788
65	Zhou, W., Jiang, Y., He, S., & Chen, D . ( 2010). Olfaction modulates visual perception in binocular rivalry. Current Biology, 20( 15), 1356-1358. doi: 10.1016/j.cub.2010.05.059 URL pmid: 20598540
66	Zuo, X. N., Martino, A. D., Kelly, C., Shehzad, Z. E., Gee, D. G., Klein, D. F., & Milham, M. P . ( 2010). The oscillating brain: Complex and reliable. NeuroImage, 49( 2), 1432-1445.
67	Zuo, X. N., & Xing, X. X. ( 2014). Test-retest reliabilities of resting-state fMRI measurements in human brain functional connectomics: A systems neuroscience perspective. Neuroscience and Biobehavioral Reviews, 45, 100-118. doi: 10.1016/j.neubiorev.2014.05.009 URL pmid: 24875392