Abstract
Spatial proximity of signals from different sensory modalities is known to be a crucial factor in facilitating efficient multisensory processing in young adults. However, recent studies have demonstrated that older adults exhibit strong visuotactile interactions even when the visual stimuli were presented in a spatially disparate position from a tactile stimulus. This suggests that visuotactile peripersonal space differs between older and younger adults. In the present study, we investigated to what extent peripersonal space expands in the sagittal direction and whether this expansion was linked to the decline in sensorimotor functions in older adults. Vibrotactile stimuli were delivered either to the left or right index finger, while visual stimuli were presented at a distance of 5 cm (near), 37.5 cm (middle), or 70 cm (far) from each finger. The participants had to respond rapidly to a randomized sequence of unimodal (visual or tactile) and simultaneous visuotactile targets (i.e., a redundant target paradigm). Sensorimotor functions were independently assessed by the Timed Up and Go (TUG) and postural stability tests. Results showed that reaction times to the visuotactile bimodal stimuli were significantly faster than those to the unimodal stimuli, irrespective of age group [younger adults: 22.0 ± 0.6 years, older adults: 75.0 ± 3.3 years (mean ± SD)] and target distance. Of importance, a race model analysis revealed that the co-activation model (i.e., visuotactile multisensory integrative process) is supported in the far condition especially for older adults with relatively poor performance on the TUG or postural stability tests. These results suggest that aging can change visuotactile peripersonal space and that it may be closely linked to declines in sensorimotor functions related to gait and balance in older adults.
Notes
Although the laterality of the effects was beyond the scope of the present study and the number of trials on each side in each condition was very small (only ten per participant), we tried to investigate laterality with the current data for supplemental information. The results of this analysis revealed that redundant target effects occurred especially on the left side, near condition in the young/old comparison data, and near and middle conditions for the TUG and postural sway classification data. Considering all participants were right-handed, handedness might affect the RTEs somehow. Unfortunately, we did not perform the race model analysis because the number of RT data per condition was too small.
References
Arbuthnott K, Frank J (2000a) Executive control in set switching: residual switch cost and task-set inhibition. Can J Exp Psychol 54:33–41
Arbuthnott K, Frank J (2000b) Trail making test, part B as a measure of executive control: validation using a set-switching paradigm. J Clin Exp Neuropsychol 22(4):518–528
Baltes PB, Lindenberger U (1997) Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? Psychol Aging 12:12–21. doi:10.1037/0882-7974.12.1.12
Barrett MM, Doheny EP, Setti A, Maguinness C, Foran TG, Kenny RA, Newell FN (2013) Reduced vision selectively impairs spatial updating in fall-prone older adults. Multisens Res 26:69–94. doi:10.1163/22134808-00002412
Bedard G, Barnett-Cowan M (2016) Impaired timing of audiovisual events in the elderly. Exp Brain Res 231:331–340. doi:10.1007/s00221-015-4466-7
Berard J, Fung J, Lamontagne A (2012) Impact of aging on visual reweighting during locomotion. Clin Neurophysiol 123:1422–1428. doi:10.1016/j.clinph.2011.11.081
Berti A, Frassinetti F (2000) When far becomes near: remapping of space by tool use. J Cogn Neurosci 12:415–420. doi:10.1162/089892900562237
Bloesch EK, Davoli CC, Abrams RA (2013) Age-related changes in attentional reference frames for peripersonal space. Psychol Sci 24:557–561. doi:10.1177/0956797612457385
Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436. doi:10.1163/156856897X00357
Bremmer F, Schlack A, Duhamel JR, Graf W, Fink GR (2001) Space coding in primate posterior parietal cortex. Neuroimage 14:S46–S51. doi:10.1006/nimg.2001.0817
Brooks CJ, Anderson AJ, Roach NW, McGraw PV, McKendrick AM (2015) Age-related changes in auditory and visual interactions in temporal rate perception. J Vis 15:2. doi:10.1167/15.16.2
Brozzoli C, Pavani F, Urquizar C, Cardinali L, Farnè A (2009) Grasping actions remap peripersonal space. Neuroreport 20:913–917. doi:10.1097/WNR.0b013e32832c0b9b
Brozzoli C, Cardinali L, Pavani F, Farnè A (2010) Action-specific remapping of peripersonal space. Neuropsychologia 48:796–802. doi:10.1016/j.neuropsychologia.2009.10.009
Bugnariu N, Fung J (2007) Aging and selective sensorimotor strategies in the regulation of upright balance. J Neuroeng Rehabil 4:19. doi:10.1186/1743-0003-4-19
Chan YM, Pianta MJ, McKendrick AM (2014) Reduced audiovisual recalibration in the elderly. Front Aging Neurosci 6:226. doi:10.3389/fnagi.2014.00226
Colonius H, Diederich A (2006) The race model inequality: interpreting a geometric measure of the amount of violation. Psychol Rev 113(1):148–154
Couth S, Gowen E, Poliakoff E (2016) Investigating the spatial and temporal modulation of visuotactile interactions in older adults. Exp Brain Res 234:1233–1248. doi:10.1007/s00221-015-4431-5
DeLoss DJ, Pierce RS, Andersen GJ (2013) Multisensory integration, aging, and the sound-induced flash illusion. Psychol Aging 28:802–812. doi:10.1037/a0033289
di Pellegrino G, Làdavas E, Farnè A (1997) Seeing where your hands are. Nature 388:730. doi:10.1038/41921
Diederich A, Colonius H, 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
Donoghue OA, Horgan NF, Savva GM, Cronin H, O’Regan C, Kenny RA (2012) Association between timed up-and-go and memory, executive function, and processing speed. J Am Geriatr Soc 60:1681–1686. doi:10.1111/j.1532-5415.2012.04120.x
Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136
Eikema DJ, Hatzitaki V, Konstantakos V, Papaxanthis C (2013) Elderly adults delay proprioceptive reweighting during the anticipation of collision avoidance when standing. Neuroscience 234:22–30. doi:10.1016/j.neuroscience.2012.12.053
Farnè A, Làdavas E (2000) Dynamic size-change of hand peripersonal space fol- lowing tool use. Neuroreport 11:1645–1649. doi:10.1348/174866407X180846
Fiacconi CM, Harvey EC, Sekuler AB, Bennett PJ (2013) The influence of aging on audiovisual temporal order judgments. Exp Aging Res 39(2):179–193. doi:10.1080/0361073X.2013.761896
Fogassi L, Gallese V, Fadiga L, Luppino G, Matelli M, Rizzolatti G (1996) Coding of peripersonal space in inferior premotor cortex (area F4). J Neurophysiol 76:141–157
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198. doi:10.1016/0022-3956(75)90026-6
Foreman M, Fletcher K, Mion L, Simon C (1996) Assessing cognitive function. Geriatr Nurs 17:228–233. doi:10.1016/S0197-4572(96)80210-2
Forster B, Cavina-Pratesi C, Aglioti SM, Berlucchi G (2002) Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time. Exp Brain Res 143:480–487. doi:10.1007/s00221-002-1017-9
Fraz JR, Francis CA, Allen MS, O’Connor SM, Thelen DG (2015) Advanced age brings a greater reliance on visual feedback to maintain balance during walking. Hum Mov Sci 40:381–392. doi:10.1016/j.humov.2015.01.012
Gaudino EA, Geisler MW, Squires NK (1995) Construct validity in the trail making test: what makes part B harder? J Clin Exp Neuropsychol 17(4):529–535
Geerligs L, Saliasi E, Renken RJ, Maurits NM, Lorist MM (2014) Flexible connectivity in the aging brain revealed by task modulations. Hum Brain Mapp 35:3788–3804. doi:10.1002/hbm.22437
Geerligs L, Renken RJ, Saliasi E, Maurits NM, Lorist MM (2015) A brain-wide study of age-related changes in functional connectivity. Cereb Cortex 25:1987–1999. doi:10.1093/cercor/bhu012
Girard S, Collignon O, Lepore F (2011) Multisensory gain within and across hemispaces in simple and choice reaction time paradigms. Exp Brain Res 214:1–8. doi:10.1007/s00221-010-2515-9
Gondan M, Minakata K (2016) A tutorial on testing the race model inequality. Atten Percept Psychophys 78(3):723–735
Graziano MS, Cooke DF (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44:2621–2635. doi:10.1016/j.neuropsychologia.2005.09.009
Graziano MS, Gross CG (1993) A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields. Exp Brain Res 97:96–109. doi:10.1007/BF00228820
Graziano MS, Yap GS, Gross CG (1994) Coding of visual space by premotor neurons. Science 266:1054–1057. doi:10.1126/science.7973661
Graziano MS, Hu XT, Gross CG (1997) Visuospatial properties of ventral premotor cortex. J Neurophysiol 77:2268–2292
Holmes NP, Spence C (2004) The body schema and the multisensory representation(s) of peripersonal space. Cogn Process 5(2):94–105. doi:10.1007/s10339-004-0013-3
Holmes NP, Calvert GA, Spence C (2004) Extending or projecting peripersonal space with tools? Multisensory interactions highlight only the distal and proximal ends of tools. Neurosci Lett 372:62–67. doi:10.1016/j.neulet.2004.09.024
Horak FB, Macpherson JM (1996) Postural orientation and equilibrium. In: Rowell LB, Shepard JT (eds) Handbook of physiology: section 12, exercise regulation and integration of multiple systems. Oxford University Press, New York, pp 255–292
Horak FB, Shupert CL, Mirka A (1989) Components of postural dyscontrol in the elderly: a review. Neurobiol Aging 10:727–738. doi:10.1016/0197-4580(89)90010-9
Howcroft J, Lemaire ED, Kofman J, McIlroy WE (2017) Elderly fall risk prediction using static posturography. PLoS One 12:e0172398. doi:10.1371/journal.pone.0172398
Hu MH, Woollacott MH (1994a) Multisensory training of standing balance in older adults: I. Postural stability and one-leg stance balance. J Gerontol 49:M52–M61
Hu MH, Woollacott MH (1994b) Multisensory training of standing balance in older adults: II. Kinematic and electromyographic postural responses. J Gerontol 49:M62–M71
Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurons. Neuroreport 7:2325–2330. doi:10.1097/00001756-199610020-00010
Jeka JJ, Allison LK, Kiemel T (2010) The dynamics of visual reweighting in healthy and fall-prone older adults. J Mot Behav 42:97–208. doi:10.1080/00222895.2010.481693
Kawagoe T, Sekiyama K (2014) Visually encoded working memory is closely associated with mobility in older adults. Exp Brain Res 232:2035–2043. doi:10.1007/s00221-014-3893-1
Kiesel A, Miller J, Ulrich R (2007) Systematic biases and type I error accumulation in tests of the race model inequality. Behav Res Methods 39:539–551
Kleiner M, Brainard D, Pelli D (2007) What’s new in Psychtoolbox-3? Perception 36 (ECVP Abstract Suppl 14)
Kristensen MT, Foss NB, Kehlet H (2007) Timed “up & go” test as a predictor of falls within 6 months after hip fracture surgery. Phys Ther 87:24–30. doi:10.2522/ptj.20050271
Làdavas E, Farnè A (2004a) Neuropsychological evidence for multimodal representations of space near specific body parts. In: Driver J, Spence C (eds) Crossmodal space and crossmodal attention. Oxford University Press, New York, pp 69–98
Làdavas E, Farnè A (2004b) Visuo-tactile representation of near-the-body space. J Physiol Paris 98:161–170. doi:10.1016/j.jphysparis.2004.03.007
Làdavas E, Serino A (2008) Action-dependent plasticity in peripersonal space representations. Cogn Neuropsychol 25:1099–1113. doi:10.1080/02643290802359113
Làdavas E, Zeloni G, Farnè A (1998a) Visual peripersonal space centred on the face in humans. Brain 121:2317–2326. doi:10.1093/brain/121.12.2317
Làdavas E, di Pellegrino G, Farnè A, Zeloni G (1998b) Neuropsychological evidence of an integrated visuotactile representation of peripersonal space in humans. J Cogn Neurosci 10:581–589. doi:10.1162/089892998562988
Laurienti PJ, Burdette JH, Maldjian JA, Wallace MT (2006) Enhanced multisensory integration in older adults. Neurobiol Aging 27:1155–1163. doi:10.1016/j.neurobiolaging.2005.05.024
Mahoney JR, Li PC, Oh-Park M, Verghese J, 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
Mahoney JR, Holtzer R, Verghese J (2014a) Visual-somatosensory integration and balance: evidence for psychophysical integrative differences in aging. Multisens Res 27:17–42. doi:10.1163/22134808-00002444
Mahoney JR, Wang C, Dumas K, Holtzer R (2014b) Visual-somatosensory integration in aging: does stimulus location really matter? Vis Neurosci 31:275–283. doi:10.1017/S0952523814000078
Mahoney JR, Dumas K, Holtzer R (2015) Visual-somatosensory integration is linked to physical activity level in older adults. Multisens Res 28:11–29. doi:10.1163/22134808-00002470
Maravita A, Husain M, Clarke K, Driver J (2001) Reaching with a tool extends visual–tactile interactions into far space: evidence from cross-modal extinction. Neuropsychologia 39:580–585. doi:10.1016/S0028-3932(00)00150-0
Maravita A, Spence C, Kennet S, Driver J (2002) Tool-use changes multimodal spatial interactions between vision and touch in normal humans. Cognition 83:B25–B34. doi:10.1016/S0010-0277(02)00003-3
McGovern DP, Roudaia E, Stapleton J, McGinnity TM, Newell FN (2014) The sound-induced flash illusion reveals dissociable age-related effects in multisensory integration. Front Aging Neurosci 6:250. doi:10.3389/fnagi.2014.00250
Merriman NA, Whyatt C, Setti A, Craig C, Newell FN (2015) Successful balance training is associated with improved multisensory function in fall-prone older adults. Comput Hum Behav 45:192–203. doi:10.1016/j.chb.2014.12.017
Miller J (1982) Divided attention evidence for coactivation with redundant signals. Cogn Psychol 14:247–279. doi:10.1016/0010-0285(82)90010-X
Miner T, Ferraro FR (1998) The role of speed of processing, inhibitory mechanisms, and presentation order in trail-making test performance. Brain Cogn 38 (2):246–253
Newell KM, Slifkin AB (1998) The nature of movement variability. In: Piek JP (ed) Motor behavior and human skill: a multidisciplinary approach. Human Kinetics, Champaign, pp 143–160
Noel JP, De Niear M, Van der Burg E, Wallace MT (2016) Audiovisual simultaneity judgment and rapid recalibration throughout the lifespan. PLoS One 11(8):e0161698. doi:10.1371/journal.pone.0161698
Park DC, Polk TA, Park R, Minear M, Savage A, Smith MR (2004) Aging reduces neural specialization in ventral visual cortex. Proc Natl Acad Sci USA 101:13091–13095. doi:10.1073/pnas.0405148101
Peiffer AM, Mozolic JL, Hugenschmidt CE, Laurienti PJ (2007) Age-related multisensory enhancement in a simple audiovisual detection task. Neuroreport 18:1077–1081. doi:10.1097/WNR.0b013e3281e72ae7
Pelli DG (1997) The videotoolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437–442. doi:10.1163/156856897X00366
Piirtola M, Era P (2006) Force platform measurements as predictors of falls among older people—a review. Gerontology 52:1–16. doi:10.1159/000089820
Podsiadlo D, Richardson S (1991) The timed “Up and Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148. doi:10.1111/j.1532-5415.1991.tb01616.x
Poliakoff E, Ashworth S, Lowe C, Spence C (2006a) Vision and touch in ageing: crossmodal selective attention and visuotactile spatial interactions. Neuropsychologia 44:507–517. doi:10.1016/j.neuropsychologia.2005.07.004
Poliakoff E, Shore DI, Lowe C, Spence C (2006b) Visuotactile temporal order judgments in ageing. Neurosci Lett 396:207–211. doi:10.1016/j.neulet.2005.11.034
Poole D, Couth S, Gowen E, Warren P, Poliakoff E (2015) Adapting the cross-modal congruency task for measuring the limits of visual-tactile interactions within and between groups. Multisens Res 28:227–224
Previc FH (1998) The neuropsychology of 3-D space. Psychol Bull 124:123–164. doi:10.1037/0033-2909.124.2.123
Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2:147–163. doi:10.1016/0166-4328(81)90053-X
Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106:655–673. doi:10.1093/brain/106.3.655
Rizzolatti G, Fadiga L, Fogassi L, Gallese V (1997) The space around us. Science 277:190–191. doi:10.1126/science.277.5323.190
Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296. doi:10.1016/S0013-4694(98)00022-4
Sambo CF, Forster B (2009) An ERP investigation on visuotactile interactions in peripersonal and extrapersonal space: evidence for the spatial rule. J Cogn Neurosci 21:1550–1559. doi:10.1162/jocn.2009.21109
Setti A, Burke KE, Kenny RA, Newell FN (2011) Is inefficient multisensory processing associated with falls in older people? Exp Brain Res 209:375–384. doi:10.1007/s00221-011-2560-z
Shams L, Kamitani Y, Shimojo S (2000) What you see is what you hear. Nature 408:6814. doi:10.1038/35048669
Shumway-Cook A, Brauer S, Woollacott M (2000) Predicting the probability for falls in community-dwelling older adults using the timed up and go test. Phys Ther 80:896–903
Spence C (2013) Just how important is spatial coincidence to multisensory integration? Evaluating the spatial rule. Ann N Y Acad Sci 1296:31–49. doi:10.1111/nyas.12121
Spence C, Pavani F, Driver J (2004) Spatial constraints on visual-tactile cross-modal distractor congruency effects. Cogn Affect Behav Neurosci 4:148–169. doi:10.3758/CABN.4.2.148
Stapleton J, Setti A, Doheny EP, Kenny RA, Newell FN (2014) A standing posture is associated with increased susceptibility to the sound-induced flash illusion in fall-prone older adults. Exp Brain Res 232:423–434. doi:10.1007/s00221-013-3750-7
Teramoto W, Kakuya T (2015) Visuotactile peripersonal space in healthy humans: evidence from crossmodal congruency and redundant target effects. Interdiscip Inf Sci 21:133–142. doi:10.4036/iis.2015.A.04
Ulrich R, Miller J, Schröter H (2007) Testing the race model inequality: an algorithm and computer programs. Behav Res Methods 39:291–302. doi:10.3758/BF03193160
Visser JE, Carpenter MG, van der Kooij H, Bloem BR (2008) The clinical utility of posturography. Clin Neurophysiol 119:2424–2436. doi:10.1016/j.clinph.2008.07.220
von Frey M (1896) Ueber den Gebrauch von Reizhaaren. In: Untersuchungen über die Sinnesfunctionen der menschlichen Haut. Erste Abhandlung: Druckempfindung und Schmerz. Abhandlungen der mathematischphysischen Classe der Königlich Sächsischen Gesellschaft der Wissenschaften, vol 23, pp 208–217
Whitney SL, Marchetti GF, Schade A, Wrisley DM (2004) The sensitivity and specificity of the Timed “Up & Go” and the Dynamic Gait Index for self-reported falls in persons with vestibular disorders. J Vestib Res 14:397–409
Yeh TT, Cluff T, Balasubramaniam R (2014) Visual reliance for balance control in older adults persists when visual information is disrupted by artificial feedback delays. PLoS One 9:e91554
Yogev-Seligmann G, Hausdorff JM, Giladi N (2009) The role of executive function and attention in gait. Mov Disord 23:329–342. doi:10.1002/mds.21720
Acknowledgements
This study was supported by JSPS KAKENHI Grant (S) (No. 16H06325), (A) (No. 25245068), and (B) (No. 26285160). Part of the data for this manuscript was presented at the International Multisensory Research Forum 2015.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Teramoto, W., Honda, K., Furuta, K. et al. Visuotactile interaction even in far sagittal space in older adults with decreased gait and balance functions. Exp Brain Res 235, 2391–2405 (2017). https://doi.org/10.1007/s00221-017-4975-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-017-4975-7