Multisensory Gains in Simple Detection Predict Global Cognition in Schoolchildren.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
04 02 2020
04 02 2020
Historique:
received:
10
05
2019
accepted:
14
01
2020
entrez:
6
2
2020
pubmed:
6
2
2020
medline:
18
11
2020
Statut:
epublish
Résumé
The capacity to integrate information from different senses is central for coherent perception across the lifespan from infancy onwards. Later in life, multisensory processes are related to cognitive functions, such as speech or social communication. During learning, multisensory processes can in fact enhance subsequent recognition memory for unisensory objects. These benefits can even be predicted; adults' recognition memory performance is shaped by earlier responses in the same task to multisensory - but not unisensory - information. Everyday environments where learning occurs, such as classrooms, are inherently multisensory in nature. Multisensory processes may therefore scaffold healthy cognitive development. Here, we provide the first evidence of a predictive relationship between multisensory benefits in simple detection and higher-level cognition that is present already in schoolchildren. Multiple regression analyses indicated that the extent to which a child (N = 68; aged 4.5-15years) exhibited multisensory benefits on a simple detection task not only predicted benefits on a continuous recognition task involving naturalistic objects (p = 0.009), even when controlling for age, but also the same relative multisensory benefit also predicted working memory scores (p = 0.023) and fluid intelligence scores (p = 0.033) as measured using age-standardised test batteries. By contrast, gains in unisensory detection did not show significant prediction of any of the above global cognition measures. Our findings show that low-level multisensory processes predict higher-order memory and cognition already during childhood, even if still subject to ongoing maturation. These results call for revision of traditional models of cognitive development (and likely also education) to account for the role of multisensory processing, while also opening exciting opportunities to facilitate early learning through multisensory programs. More generally, these data suggest that a simple detection task could provide direct insights into the integrity of global cognition in schoolchildren and could be further developed as a readily-implemented and cost-effective screening tool for neurodevelopmental disorders, particularly in cases when standard neuropsychological tests are infeasible or unavailable.
Identifiants
pubmed: 32019951
doi: 10.1038/s41598-020-58329-4
pii: 10.1038/s41598-020-58329-4
pmc: PMC7000735
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1394Références
Murray, M. M., Lewkowicz, D. J., Amedi, A. & Wallace, M. T. Multisensory Processes: A Balancing Act across the Lifespan. Trends Neurosci. 39, 567–579 (2016).
pubmed: 27282408
pmcid: 4967384
doi: 10.1016/j.tins.2016.05.003
Amso, D. & Scerif, G. The attentive brain: insights from developmental cognitive neuroscience. Nat. Rev. 16, 606–619 (2015).
doi: 10.1038/nrn4025
Stein, B. E. & Meredith, M. A. The Merging of the Senses. (MIT Press, 1993).
Murray, M. M. & Wallace, M. T. The Neural Bases of Multisensory Processes. (CRC Press, 2012).
Bahrick, L. E. & Lickliter, R. Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. Dev. Psychol. 36, 190–201 (2000).
pubmed: 10749076
pmcid: 2704001
doi: 10.1037/0012-1649.36.2.190
Bahrick, L. E. & Lickliter, R. The role of intersensory redundancy in early perceptual, cognitive, and social development. In Multisensory development (eds. Bremner, A. J., Lewkowicz, D. J. & Spence, C.) 183–206 (Oxford University Press, 2012).
Lewkowicz, D. J. & King, A. J. The developmental and evolutionary emergence of multisensory processing: From single cells to behavior. In The New Handbook of Multisensory Processing (ed. Stein, B. E.) (MIT Press, 2012).
Lewkowicz, D. J. Early experience and multisensory perceptual narrowing. Dev. Psychobiol. 56, 292–315 (2014).
pubmed: 24435505
pmcid: 3953347
doi: 10.1002/dev.21197
Matusz, P. J., Dikker, S., Huth, A. G. & Perrodin, C. Are We Ready for Real-world Neuroscience? J. Cogn. Neurosci. 1–13. https://doi.org/10.1162/jocn_e_01276 (2018).
pubmed: 29916793
doi: 10.1162/jocn_e_01276
Dionne-Dostie, E., Paquette, N., Lassonde, M. & Gallagher, A. Multisensory Integration and Child Neurodevelopment. Brain Sci. 5, 32–57 (2015).
pubmed: 25679116
pmcid: 4390790
doi: 10.3390/brainsci5010032
Baker, L. A., Vernon, P. A. & Ho, H. Z. The genetic correlation between intelligence and speed of information processing. Behav. Genet. 21, 351–367 (1991).
pubmed: 1953598
doi: 10.1007/BF01065972
Vernon, P. A., Nador, S. & Kantor, L. Reaction times and speed-of-processing: Their relationship to timed and untimed measures of intelligence. Intelligence 9, 357–374 (1985).
doi: 10.1016/0160-2896(85)90020-0
Sheppard, L. D. & Vernon, P. A. Intelligence and speed of information-processing: A review of 50 years of research. Pers. Individ. Dif. 44, 535–551 (2008).
doi: 10.1016/j.paid.2007.09.015
Vernon, P. A. & Weese, S. E. Predicting intelligence with multiple speed of information-processing tests. Pers. Individ. Dif. 14, 413–419 (1993).
doi: 10.1016/0191-8869(93)90310-Y
Park, J., Mainela-Arnold, E. & Miller, C. A. Information processing speed as a predictor of IQ in children with and without specific language impairment in grades 3 and 8. J. Commun. Disord. 53, 57–69 (2015).
pubmed: 25577725
doi: 10.1016/j.jcomdis.2014.11.002
Rose, S. A. et al. Cognitive Cascade in Infancy: Pathways from Prematurity to Later Mental Development. Intelligence 36, 367–378 (2008).
pubmed: 19122757
pmcid: 2504323
doi: 10.1016/j.intell.2007.07.003
Birch, H. G., Belmont, L., Ph, D., Belmont, L. & Ph, D. Auditory visual integration in normal and retarded readers. Bull. Ort. Soc. 15, 48–96 (1965).
doi: 10.1007/BF02653757
Birch, H. G. & Belmont, L. Auditory-Visual Integration, Intelligence and Reading Ability in School Children. Percept. Mot. Skills 20, 295–305 (1965).
pubmed: 14286542
doi: 10.2466/pms.1965.20.1.295
Birch, H. G. & Belmont, L. Auditory visual integration in normal and retarded readers. Bull. Ort. Soc. 15, 48–96 (1965).
doi: 10.1007/BF02653757
Rose, S. A., Feldman, J. F., Jankowski, J. J. & Futterweit, L. R. Visual and auditory temporal processing, cross-modal transfer, and reading. J. Learn. Disabil. 32, 256–66.
Heikkilä, J. & Tiippana, K. School-aged children can benefit from audiovisual semantic congruency during memory encoding. Exp. brain Res. 62, 123–130 (2015).
Heikkilä, J., Alho, K., Hyvönen, H. & Tiippana, K. Audiovisual semantic congruency during encoding enhances memory performance. Exp. Psychol. 62, 123–30 (2015).
pubmed: 25384643
doi: 10.1027/1618-3169/a000279
Broadbent, H. J., White, H., Mareschal, D. & Kirkham, N. Z. Incidental learning in a multisensory environment across childhood. Dev. Sci. 21, (2018).
Broadbent, H. J., Osborne, T., Mareschal, D. & Kirkham, N. Z. Withstanding the test of time: Multisensory cues improve the delayed retention of incidental learning. Dev. Sci. 1–7. https://doi.org/10.1111/desc.12726 (2018).
pubmed: 30184309
doi: 10.1111/desc.12726
Thelen, A., Matusz, P. J. P. J. & Murray, M. M. M. Multisensory context portends object memory. Curr. Biol. 24, R734–R735 (2014).
pubmed: 25137580
doi: 10.1016/j.cub.2014.06.040
Murray, M. M. et al. Sensory dominance and multisensory integration as screening tools in aging. Sci. Rep. 8, 8901 (2018).
pubmed: 29891964
pmcid: 5995929
doi: 10.1038/s41598-018-27288-2
Barutchu, A., Crewther, D. P. & Crewther, S. G. The race that precedes coactivation: Development of multisensory facilitation in children. Dev. Sci. 12, 464–473 (2009).
pubmed: 19371371
doi: 10.1111/j.1467-7687.2008.00782.x
John & Raven, J. Raven Progressive Matrices. in Handbook of Nonverbal Assessment 223–237 (Springer US, 2003). https://doi.org/10.1007/978-1-4615-0153-4_11 .
doi: 10.1007/978-1-4615-0153-4_11
Neale, M. D., McKay, M. F. & Childs, G. H. The Neale Analysis of Reading Ability - Revised. Br. J. Educ. Psychol. 56, 346–356 (1986).
doi: 10.1111/j.2044-8279.1986.tb03047.x
Barutchu, A. et al. The relationship between multisensory integration and IQ in children. Dev. Psychol. 47, 877–885 (2011).
pubmed: 21142364
doi: 10.1037/a0021903
pmcid: 21142364
Barutchu, A., Fifer, J. M., Shivdasani, M. N., Crewther, S. G. & Paolini, A. G. The Interplay Between Multisensory Associative Learning and IQ in Children. Child Dev., https://doi.org/10.1111/cdev.13210 (2019).
Barutchu, A., Sahu, A., Humphreys, G. W. & Spence, C. Multisensory processing in event-based prospective memory. Acta Psychol. (Amst). 192, 23–30 (2019).
pubmed: 30391627
doi: 10.1016/j.actpsy.2018.10.015
pmcid: 30391627
Harrar, V. et al. Multisensory integration and attention in developmental dyslexia. Curr. Biol. 24, 531–535 (2014).
pubmed: 24530067
doi: 10.1016/j.cub.2014.01.029
pmcid: 24530067
Wallace, M. T. & Stevenson, R. A. The construct of the multisensory temporal binding window and its Dysregulation in developmental Disabilities. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2014.08.005 (2014).
pubmed: 25128432
pmcid: 4326640
doi: 10.1016/j.neuropsychologia.2014.08.005
Murray, M. M. et al. Rapid discrimination of visual and multisensory memories revealed by electrical neuroimaging. Neuroimage 21, 125–135 (2004).
pubmed: 14741649
doi: 10.1016/j.neuroimage.2003.09.035
pmcid: 14741649
Lehmann, S. & Murray, M. M. The role of multisensory memories in unisensory object discrimination. Cogn. Brain Res. 24, (2005).
Murray, M. M., Foxe, J. J. & Wylie, G. R. The brain uses single-trial multisensory memories to discriminate without awareness. Neuroimage 27, 473–8 (2005).
pubmed: 15894494
doi: 10.1016/j.neuroimage.2005.04.016
pmcid: 15894494
Thelen, A., Cappe, C. & Murray, M. M. Electrical neuroimaging of memory discrimination based on single-trial multisensory learning. Neuroimage 62, 1478–1488 (2012).
pubmed: 22609795
doi: 10.1016/j.neuroimage.2012.05.027
pmcid: 22609795
Matusz, P. J. P. J. et al. The role of auditory cortices in the retrieval of single-trial auditory-visual object memories. Eur. J. Neurosci. 41, 699–708 (2015).
pubmed: 25728186
doi: 10.1111/ejn.12804
pmcid: 25728186
Thelen, A., Talsma, D. & Murray, M. M. Single-trial multisensory memories affect later auditory and visual object discrimination. Cognition 138, (2015).
Matusz, P. J., Wallace, M. T. & Murray, M. M. A multisensory perspective on object memory. Neuropsychologia 105, (2017).
Huth, M. E., Popelka, G. R. & Blevins, N. H. Comprehensive measures of sound exposures in cinemas using smart phones. Ear Hear. 35, 680–6.
Fort, A., Delpuech, C., Pernier, J. & Giard, M.-H. Dynamics of cortico-subcortical cross-modal operations involved in audio-visual object detection in humans. Cereb. Cortex 12, 1031–9 (2002).
pubmed: 12217966
doi: 10.1093/cercor/12.10.1031
Hillock, A. R., Powers, A. R. & Wallace, M. T. Binding of sights and sounds: Age-related changes in multisensory temporal processing. Neuropsychologia 49, 461–467 (2011).
pubmed: 21134385
doi: 10.1016/j.neuropsychologia.2010.11.041
Wechsler, D. Wechsler Intelligence Scale for Children and Adolescents. (2003).
Rose, S. A., Feldman, J. F. & Jankowski, J. J. The building blocks of cognition. J. Pediatr. 143, S54–61 (2003).
pubmed: 14597914
doi: 10.1067/S0022-3476(03)00402-5
Fournier, M. & Albaret, J.-M. Étalonnage des blocs de Corsi sur une population d’enfants scolarisés du CP à la 6e. Développements 16–17, 76 (2013).
doi: 10.3917/devel.016.0076
Tuddenham, R. D., Davis, L., Davison, L. & Schindler, R. An experimental group version for school children of the progressive matrices. J. Consult. Psychol. 22, 30 (1958).
pubmed: 13513870
doi: 10.1037/h0043583
Raven, J., Raven, J. & Court, H. Manual for Raven’s Progressive Matrices. (Harcourt Assessment, 2003).
Murray, M. M. & Thelen, A. The Efficacy of Single-Trial Multisensory Memories. Multisens. Res. 26, 483–502 (2013).
pubmed: 24649531
doi: 10.1163/22134808-00002416
Spence, C. & Deroy, O. How automatic are crossmodal correspondences? Conscious. Cogn. 22, 245–260 (2013).
pubmed: 23370382
doi: 10.1016/j.concog.2012.12.006
Matusz, P. J. et al. Multi-modal distraction: Insights from children’s limited attention. Cognition 136, 156–165 (2015).
pubmed: 25497524
doi: 10.1016/j.cognition.2014.11.031
Matusz, P. J., Merkley, R., Faure, M. & Scerif, G. Expert attention: Attentional allocation depends on the differential development of multisensory number representations. Cognition 186, 171–177 (2019).
pubmed: 30782550
doi: 10.1016/j.cognition.2019.01.013
Miller, J. Divided attention: evidence for coactivation with redundant signals. Cogn. Psychol. 14, 247–79 (1982).
pubmed: 7083803
doi: 10.1016/0010-0285(82)90010-X
Hughes, H. C., Reuter-Lorenz, P. A., Nozawa, G. & Fendrich, R. Visual-auditory interactions in sensorimotor processing: saccades versus manual responses. J. Exp. Psychol. Hum. Percept. Perform. 20, 131–53 (1994).
pubmed: 8133219
doi: 10.1037/0096-1523.20.1.131
Kiesel, A., Miller, J. & Ulrich, R. Systematic biases and Type i error accumulation in tests of the race model inequality. Behav. Res. Methods 39, 539–551 (2007).
pubmed: 17958166
doi: 10.3758/BF03193024
Gondan, M. & Minakata, K. A tutorial on testing the race model inequality. Attention, Perception, Psychophys. 78, 723–735 (2016).
doi: 10.3758/s13414-015-1018-y
Sperdin, H. F., Cappe, C., Foxe, J. J. & Murray, M. M. Early, low-level auditory-somatosensory multisensory interactions impact reaction time speed. Front. Integr. Neurosci. 3, 2 (2009).
pubmed: 19404410
pmcid: 2659167
doi: 10.3389/neuro.07.002.2009
Murray, M. M., Foxe, J. J., Higgins, B. A., Javitt, D. C. & Schroeder, C. E. Visuo-spatial neural response interactions in early cortical processing during a simple reaction time task: a high-density electrical mapping study. Neuropsychologia 39, 828–44 (2001).
pubmed: 11369406
doi: 10.1016/S0028-3932(01)00004-5
Rijsdijk, F. V., Vernon, P. A. & Boomsma, D. I. The genetic basis of the relation between speed-of-information- processing and IQ. Behav. Brain Res. 95, 77–84 (1998).
pubmed: 9754879
doi: 10.1016/S0166-4328(97)00212-X
Vernon, P. A. Speed of Information Processing and Intelligence. (Ablex Publishing, 1987).
Jensen, A. R. Reaction Time and Psychometric g. In A Model for Intelligence 93–132 (Springer Berlin Heidelberg, 1982). https://doi.org/10.1007/978-3-642-68664-1_4 .
doi: 10.1007/978-3-642-68664-1_4
Murray, M. M., Thelen, A., Ionta, S. & Wallace, M. T. Contributions of intra- and inter- individual differences to multisensory processes. J. Cogn. Neurosci. (2018).
Neel, M. L. et al. Randomized controlled trial protocol to improve multisensory neural processing, language and motor outcomes in preterm infants. BMC Pediatr. 19, 81 (2019).
pubmed: 30890132
pmcid: 6423745
doi: 10.1186/s12887-019-1455-1
Fry, A. F. & Hale, S. Processing speed, working memory, and fluid intelligence. Psychol. Sci. 7, 237–241 (1996).
doi: 10.1111/j.1467-9280.1996.tb00366.x
Shams, L. & Seitz, A. R. Benefits of multisensory learning. Trends Cogn. Sci. 12, 411–7 (2008).
pubmed: 18805039
doi: 10.1016/j.tics.2008.07.006
Powers, A. R., Hillock, A. R. & Wallace, M. T. Perceptual training narrows the temporal window of multisensory binding. J. Neurosci. 29, 12265–74 (2009).
pubmed: 19793985
pmcid: 2771316
doi: 10.1523/JNEUROSCI.3501-09.2009
Powers, A. R., Hillock-Dunn, A. & Wallace, M. T. Generalization of multisensory perceptual learning. Sci. Rep. 6, 1–9 (2016).
doi: 10.1038/s41598-016-0001-8
Stevenson, R. A. et al. Multisensory temporal integration in autism spectrum disorders. J Neurosci 34, 691–697 (2014).
pubmed: 24431427
pmcid: 3891950
doi: 10.1523/JNEUROSCI.3615-13.2014
Poliakoff, E., Shore, D. I., Lowe, C. & Spence, C. Visuotactile temporal order judgments in ageing. Neurosci. Lett. 396, 207–11 (2006).
pubmed: 16356634
doi: 10.1016/j.neulet.2005.11.034
pmcid: 16356634
Stevenson, R. A., Wallace, M. T. & Altieri, N. The interaction between stimulus factors and cognitive factors during multisensory integration of audiovisual speech. Front. Psychol. 5, 352 (2014).
pubmed: 24817856
pmcid: 4013471
Murray, M. M., Matusz, P. J. & Amedi, A. Neuroplasticity: Unexpected Consequences of Early Blindness. Curr. Biol. 25, (2015).
Montessori, M. The Secret of Childhood. (Ballantine Books, 1982).
Lillard, A. S. et al. Montessori preschool elevates and equalizes child outcomes: A longitudinal study. Front. Psychol. 8, 1–19 (2017).
doi: 10.3389/fpsyg.2017.01783
Lillard, A. THE EARLY YEARS: Evaluating Montessori Education. Science (80-.). 313, 1893–1894 (2006).
doi: 10.1126/science.1132362
Denervaud, S., Knebel, J.F., Hagmann, P. & Gentaz, E. Beyond executive functions, creativity skills benefit academic outcomes: Insights from Montessori education. PLoS One 14, e0225319 (2019).
Hecht, D., Reiner, M. & Karni, A. Multisensory enhancement: gains in choice and in simple response times. Exp. Brain Res. 189, 133–43 (2008).
pubmed: 18478210
doi: 10.1007/s00221-008-1410-0
pmcid: 18478210
Romei, V., Murray, M. M., Merabet, L. B. & Thut, G. Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: implications for multisensory interactions. J. Neurosci. 27, 11465–72 (2007).
pubmed: 17959789
pmcid: 6673223
doi: 10.1523/JNEUROSCI.2827-07.2007
Martuzzi, R. et al. Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb. Cortex 17, 1672–9 (2007).
pubmed: 16968869
doi: 10.1093/cercor/bhl077
pmcid: 16968869
Molholm, S. et al. Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res. Cogn. Brain Res. 14, 115–28 (2002).
pubmed: 12063135
doi: 10.1016/S0926-6410(02)00066-6
Brandwein, A. B. et al. The Development of Multisensory Integration in High-Functioning Autism: High-Density Electrical Mapping and Psychophysical Measures Reveal Impairments in the Processing of Audiovisual Inputs. Cereb. Cortex. https://doi.org/10.1093/cercor/bhs109 (2012).
pubmed: 22628458
doi: 10.1093/cercor/bhs109
Otto, T. U., Dassy, B. & Mamassian, P. Principles of multisensory behavior. J. Neurosci. 33, 7463–74 (2013).
pubmed: 23616552
pmcid: 6619564
doi: 10.1523/JNEUROSCI.4678-12.2013
Hahn, N., Foxe, J. J. & Molholm, S. Impairments of multisensory integration and cross-sensory learning as pathways to dyslexia. Neurosci. Biobehav. Rev. 47, 384–392 (2014).
pubmed: 25265514
doi: 10.1016/j.neubiorev.2014.09.007
Stevenson, R. A. et al. The cascading influence of multisensory processing on speech perception in autism. Autism 22, 609–624 (2018).
pubmed: 28506185
doi: 10.1177/1362361317704413
Snodgrass, J. G. & Vanderwart, M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J. Exp. Psychol. Hum. Learn. 6, 174–215 (1980).
pubmed: 7373248
doi: 10.1037/0278-7393.6.2.174