Subscribe to RSS
DOI: 10.1055/s-0043-1770137
Age-Related Changes in Temporal Binding Involving Auditory and Vestibular Inputs
FUNDING/ACKNOWLEDGMENTS This work was supported by NIH R01DC017425 and VA RR&D I50RX002361 (M.E.H., T.E.H.); the Doris Duke Charitable Foundation (A.K.M.); VA RR&D C9230C (M.E.H., T.E.H.), and NIH T35DC008765 (S.B.S.). This material is the result of work supported with resources and the use of facilities at the VA Rehabilitation Research and Development (RR&D) National Center for Rehabilitative Auditory Research (NCRAR) (Center Award #C2361C/I50 RX002361) at the VA Portland Health Care System in Portland, Oregon.Abstract
Maintaining balance involves the combination of sensory signals from the visual, vestibular, proprioceptive, and auditory systems. However, physical and biological constraints ensure that these signals are perceived slightly asynchronously. The brain only recognizes them as simultaneous when they occur within a period of time called the temporal binding window (TBW). Aging can prolong the TBW, leading to temporal uncertainty during multisensory integration. This effect might contribute to imbalance in the elderly but has not been examined with respect to vestibular inputs. Here, we compared the vestibular-related TBW in 13 younger and 12 older subjects undergoing 0.5 Hz sinusoidal rotations about the earth-vertical axis. An alternating dichotic auditory stimulus was presented at the same frequency but with the phase varied to determine the temporal range over which the two stimuli were perceived as simultaneous at least 75% of the time, defined as the TBW. The mean TBW among younger subjects was 286 ms (SEM ± 56 ms) and among older subjects was 560 ms (SEM ± 52 ms). TBW was related to vestibular sensitivity among younger but not older subjects, suggesting that a prolonged TBW could be a mechanism for imbalance in the elderly person independent of changes in peripheral vestibular function.
Keywords
motion perception - reaction time - rotation - time factors - proprioception/physiology - sensory thresholds/physiology - vestibule - labyrinth/physiologyPublication History
Article published online:
22 June 2023
© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)
Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA
-
References
- 1 Green AM, Angelaki DE. Multisensory integration: resolving sensory ambiguities to build novel representations. Curr Opin Neurobiol 2010; 20 (03) 353-360
- 2 Jeka JJ, Allison LK, Kiemel T. The dynamics of visual reweighting in healthy and fall-prone older adults. J Mot Behav 2010; 42 (04) 197-208
- 3 Ernst MO, Bülthoff HH. Merging the senses into a robust percept. Trends Cogn Sci 2004; 8 (04) 162-169
- 4 Spence C, Squire S. Multisensory integration: maintaining the perception of synchrony. Curr Biol 2003; 13 (13) R519-R521
- 5 Vroomen J, Keetels M. Perception of intersensory synchrony: a tutorial review. Atten Percept Psychophys 2010; 72 (04) 871-884
- 6 Yaguchi A, Hidaka S. Distinct autistic traits are differentially associated with the width of the multisensory temporal binding window. Multisens Res 2018; 31 (06) 523-536
- 7 Zhou HY, Cai XL, Weigl M, Bang P, Cheung EFC, Chan RCK. Multisensory temporal binding window in autism spectrum disorders and schizophrenia spectrum disorders: a systematic review and meta-analysis. Neurosci Biobehav Rev 2018; 86: 66-76
- 8 Stevenson RA, Siemann JK, Schneider BC. et al. Multisensory temporal integration in autism spectrum disorders. J Neurosci 2014; 34 (03) 691-697
- 9 Hairston WD, Burdette JH, Flowers DL, Wood FB, Wallace MT. Altered temporal profile of visual-auditory multisensory interactions in dyslexia. Exp Brain Res 2005; 166 (3-4): 474-480
- 10 Meilleur A, Foster NEV, Coll SM, Brambati SM, Hyde KL. Unisensory and multisensory temporal processing in autism and dyslexia: a systematic review and meta-analysis. Neurosci Biobehav Rev 2020; 116: 44-63
- 11 Stevenson RA, Park S, Cochran C. et al. The associations between multisensory temporal processing and symptoms of schizophrenia. Schizophr Res 2017; 179: 97-103
- 12 Panagiotidi M, Overton PG, Stafford T. Multisensory integration and ADHD-like traits: Evidence for an abnormal temporal integration window in ADHD. Acta Psychol (Amst) 2017; 181: 10-17
- 13 Scarpina F, Migliorati D, Marzullo P, Mauro A, Scacchi M, Costantini M. Altered multisensory temporal integration in obesity. Sci Rep 2016; 6 (01) 28382
- 14 Zmigrod L, Zmigrod S. On the temporal precision of thought: individual differences in the multisensory temporal binding window predict performance on verbal and nonverbal problem solving tasks. Multisens Res 2016; 29: 679-701
- 15 Dinnerstein AJ, Zlotogura P. Intermodal perception of temporal order and motor skills: effects of age. Percept Mot Skills 1968; 26 (03) 987-1000
- 16 Poliakoff E, Shore DI, Lowe C, Spence C. Visuotactile temporal order judgments in ageing. Neurosci Lett 2006; 396 (03) 207-211
- 17 Setti A, Burke KE, Kenny RA, Newell FN. Is inefficient multisensory processing associated with falls in older people?. Exp Brain Res 2011; 209 (03) 375-384
- 18 Bedard G, Barnett-Cowan M. Impaired timing of audiovisual events in the elderly. Exp Brain Res 2016; 234 (01) 331-340
- 19 Stevenson RA, Baum SH, Krueger J, Newhouse PA, Wallace MT. Links between temporal acuity and multisensory integration across life span. J Exp Psychol Hum Percept Perform 2018; 44 (01) 106-116
- 20 Lupo J, Barnett-Cowan M. Impaired perceived timing of falls in the elderly. Gait Posture 2018; 59: 40-45
- 21 Stapleton J, Setti A, Doheny EP, Kenny RA, Newell FN. A standing posture is associated with increased susceptibility to the sound-induced flash illusion in fall-prone older adults. Exp Brain Res 2014; 232 (02) 423-434
- 22 Sanders MC, Chang NYN, Hiss MM, Uchanski RM, Hullar TE. Temporal binding of auditory and rotational stimuli. Exp Brain Res 2011; 210 (3-4): 539-547
- 23 Chang NYN, Uchanski RM, Hullar TE. Temporal integration of auditory and vestibular stimuli. Laryngoscope 2012; 122 (06) 1379-1384
- 24 Lubetzky AV, Gospodarek M, Arie L, Kelly J, Roginska A, Cosetti M. Auditory input and postural control in adults: a narrative review. JAMA Otolaryngol Head Neck Surg 2020; 146 (05) 480-487
- 25 Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther 2000; 80 (09) 896-903
- 26 Marme-Karelse AM, Bles W. Circular vection and human posture, II. Does the auditory system play a role?. Agressologie 1977; 18 (06) 329-333
- 27 Lewald J, Karnath HO. Vestibular influence on human auditory space perception. J Neurophysiol 2000; 84 (02) 1107-1111
- 28 Shayman CS, Peterka RJ, Gallun FJ, Oh Y, Chang NN, Hullar TE. Frequency-dependent integration of auditory and vestibular cues for self-motion perception. J Neurophysiol 2020; 123 (03) 936-944
- 29 Katzman R, Brown T, Fuld P, Peck A, Schechter R, Schimmel H. Validation of a short Orientation-Memory-Concentration Test of cognitive impairment. Am J Psychiatry 1983; 140 (06) 734-739
- 30 Mallery RM, Olomu OU, Uchanski RM, Militchin VA, Hullar TE. Human discrimination of rotational velocities. Exp Brain Res 2010; 204 (01) 11-20
- 31 Powers III AR, Hillock AR, Wallace MT. Perceptual training narrows the temporal window of multisensory binding. J Neurosci 2009; 29 (39) 12265-12274
- 32 Hillock AR, Powers AR, Wallace MT. Binding of sights and sounds: age-related changes in multisensory temporal processing. Neuropsychologia 2011; 49 (03) 461-467
- 33 Hirsh IJ, Fraisse P. [Simultaneous character and succession of heterogenous stimuli]. Annee Psychol 1964; 64: 1-19
- 34 Dixon NF, Spitz L. The detection of auditory visual desynchrony. Perception 1980; 9 (06) 719-721
- 35 Slutsky DA, Recanzone GH. Temporal and spatial dependency of the ventriloquism effect. Neuroreport 2001; 12 (01) 7-10
- 36 Lewald J, Guski R. Cross-modal perceptual integration of spatially and temporally disparate auditory and visual stimuli. Brain Res Cogn Brain Res 2003; 16 (03) 468-478
- 37 Zampini M, Guest S, Shore DI, Spence C. Audio-visual simultaneity judgments. Percept Psychophys 2005; 67 (03) 531-544
- 38 Bohannon RW. Reference values for the timed up and go test: a descriptive meta-analysis. J Geriatr Phys Ther 2006; 29 (02) 64-68
- 39 Kristensen MT, Foss NB, Kehlet H. Timed “up & go” test as a predictor of falls within 6 months after hip fracture surgery. Phys Ther 2007; 87 (01) 24-30
- 40 Virsu V, Lahti-Nuuttila P, Laasonen M. Crossmodal temporal processing acuity impairment aggravates with age in developmental dyslexia. Neurosci Lett 2003; 336 (03) 151-154
- 41 Diederich A, Colonius H. eds. Crossmodal interaction in speeded responses: time window of integration model. In: Progress in Brain Research. Vol 174. Elsevier; 2009: 119-135
- 42 Salthouse TA, Somberg BL. Isolating the age deficit in speeded performance. J Gerontol 1982; 37 (01) 59-63
- 43 Kail R, Salthouse TA. Processing speed as a mental capacity. Acta Psychol (Amst) 1994; 86 (2-3): 199-225
- 44 Furman JM, Müller MLTM, Redfern MS, Jennings JR. Visual-vestibular stimulation interferes with information processing in young and older humans. Exp Brain Res 2003; 152 (03) 383-392
- 45 Brandt T, Bartenstein P, Janek A, Dieterich M. Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain 1998; 121 (Pt 9): 1749-1758
- 46 Wallace MT, Stein BE. Development of multisensory neurons and multisensory integration in cat superior colliculus. J Neurosci 1997; 17 (07) 2429-2444
- 47 Binns KE, Salt TE. Importance of NMDA receptors for multimodal integration in the deep layers of the cat superior colliculus. J Neurophysiol 1996; 75 (02) 920-930
- 48 Huang L, Pallas SL. NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression. J Neurophysiol 2001; 86 (03) 1179-1194
- 49 Newcomer JW, Farber NB, Olney JW. NMDA receptor function, memory, and brain aging. Dialogues Clin Neurosci 2000; 2 (03) 219-232
- 50 Hirokawa J, Bosch M, Sakata S, Sakurai Y, Yamamori T. Functional role of the secondary visual cortex in multisensory facilitation in rats. Neuroscience 2008; 153 (04) 1402-1417
- 51 Rissman RA, Bennett DA, Armstrong DM. Subregional analysis of GABA(A) receptor subunit mRNAs in the hippocampus of older persons with and without cognitive impairment. J Chem Neuroanat 2004; 28 (1-2): 17-25
- 52 Shayman CS, Seo JH, Oh Y, Lewis RF, Peterka RJ, Hullar TE. Relationship between vestibular sensitivity and multisensory temporal integration. J Neurophysiol 2018; 120 (04) 1572-1577
- 53 Brooks CJ, Chan YM, Anderson AJ, McKendrick AM. Audiovisual temporal perception in aging: the role of multisensory integration and age-related sensory loss. Front Hum Neurosci 2018; 12: 192
- 54 Hugenschmidt CE, Mozolic JL, Tan H, Kraft RA, Laurienti PJ. Age-related increase in cross-sensory noise in resting and steady-state cerebral perfusion. Brain Topogr 2009; 21 (3-4): 241-251
- 55 Angelaki DE, Cullen KE. Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 2008; 31 (01) 125-150
- 56 Stevens MN, Barbour DL, Gronski MP, Hullar TE. Auditory contributions to maintaining balance. J Vestib Res 2016; 26 (5-6): 433-438
- 57 Foucher JR, Lacambre M, Pham BT, Giersch A, Elliott MA. Low time resolution in schizophrenia Lengthened windows of simultaneity for visual, auditory and bimodal stimuli. Schizophr Res 2007; 97 (1-3): 118-127
- 58 Başkent D, Bazo D. Audiovisual asynchrony detection and speech intelligibility in noise with moderate to severe sensorineural hearing impairment. Ear Hear 2011; 32 (05) 582-592
- 59 Foss-Feig JH, Kwakye LD, Cascio CJ. et al. An extended multisensory temporal binding window in autism spectrum disorders. Exp Brain Res 2010; 203 (02) 381-389
- 60 Lee H, Noppeney U. Long-term music training tunes how the brain temporally binds signals from multiple senses. Proc Natl Acad Sci U S A 2011; 108 (51) E1441-E1450
- 61 Fujisaki W, Shimojo S, Kashino M, Nishida S. Recalibration of audiovisual simultaneity. Nat Neurosci 2004; 7 (07) 773-778
- 62 Navarra J, Vatakis A, Zampini M, Soto-Faraco S, Humphreys W, Spence C. Exposure to asynchronous audiovisual speech extends the temporal window for audiovisual integration. Brain Res Cogn Brain Res 2005; 25 (02) 499-507
- 63 Stevenson RA, Wilson MM, Powers AR, Wallace MT. The effects of visual training on multisensory temporal processing. Exp Brain Res 2013; 225 (04) 479-489
- 64 Vatakis A, Navarra J, Soto-Faraco S, Spence C. Audiovisual temporal adaptation of speech: temporal order versus simultaneity judgments. Exp Brain Res 2008; 185 (03) 521-529
- 65 Sugano Y, Keetels M, Vroomen J. Adaptation to motor-visual and motor-auditory temporal lags transfer across modalities. Exp Brain Res 2010; 201 (03) 393-399
- 66 Petrini K, Dahl S, Rocchesso D. et al. Multisensory integration of drumming actions: musical expertise affects perceived audiovisual asynchrony. Exp Brain Res 2009; 198 (2-3): 339-352