Skip to main content
Log in

Effect of anticipatory multisensory integration on sensory–motor performance

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Multisensory integration (MSI) is a phenomenon that occurs in sensory areas after the presentation of multimodal stimuli. Nowadays, little is known about the anticipatory top-down processes taking place in the preparation stage of processing before the stimulus onset. Considering that the top-down modulation of modality-specific inputs might affect the MSI process, this study attempts to understand whether the direct modulation of the MSI process, beyond the well-known sensory effects, may lead to additional changes in multisensory processing also in non-sensory areas (i.e., those related to task preparation and anticipation). To this aim, event-related potentials (ERPs) were analyzed both before and after auditory and visual unisensory and multisensory stimuli during a discriminative response task (Go/No-go type). Results showed that MSI did not affect motor preparation in premotor areas, while cognitive preparation in the prefrontal cortex was increased and correlated with response accuracy. Early post-stimulus ERP activities were also affected by MSI and correlated with response time. Collectively, the present results point to the plasticity accommodating nature of the MSI processes, which are not limited to perception and extend to anticipatory cognitive preparation for task execution. Further, the enhanced cognitive control emerging during MSI is discussed in the context of Bayesian accounts of augmented predictive processing related to increased perceptual uncertainty.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Beauchamp MS (2005) Statistical criteria in fMRI studies of multisensory integration. Neuroinformatics 3:93–113

    Article  PubMed  PubMed Central  Google Scholar 

  • Beauchamp MS, Lee KE, Argall BD, Martin A (2004) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823

    Article  CAS  PubMed  Google Scholar 

  • Berchicci M, Lucci G, Pesce C, Spinelli D, Di Russo F (2012) Prefrontal hyperactivity in older people during motor planning. Neuroimage 62(3):1750–1760

    Article  PubMed  Google Scholar 

  • Berchicci M, Pontifex MB, Drollette ES, Pesce C, Hillman CH, Di Russo F (2015) From cognitive motor preparation to visual processing: the benefits of childhood fitness to brain health. Neuroscience 298:211–219

    Article  CAS  PubMed  Google Scholar 

  • Berchicci M, Spinelli D, Di Russo F (2016) New insights into old waves. Matching stimulus-and response-locked ERPs on the same time-window. Biol Psychol 117:202–215

    Article  CAS  PubMed  Google Scholar 

  • Berchicci M, Ten Brink AF, Quinzi F, Perri RL, Spinelli D, Di Russo F (2019) Electrophysiological evidence of sustained spatial attention effects over anterior cortex: possible contribution of the anterior insula. Psychophysiology 56(7):e13369

    Article  PubMed  Google Scholar 

  • Bianco V, Perri RL, Berchicci M, Quinzi F, Spinelli D, Di Russo F (2020a) Modality-specific sensory readiness for upcoming events revealed by slow cortical potentials. Brain Struct Funct 225(1):149–159

    Article  CAS  PubMed  Google Scholar 

  • Bianco V, Berchicci M, Livio Perri R, Quinzi F, Mussini E, Spinelli D, Di Russo F (2020b) Preparatory ERPs in visual, auditory, and somatosensory discriminative motor tasks. Psychophysiology 57(12):e13687

    Article  PubMed  Google Scholar 

  • Busse L, Roberts KC, Crist RE, Weissman DH, Woldorff MG (2005) The spread of attention across modalities and space in a multisensory object. Proc Natl Acad Sci 102(51):18751–18756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvert GA, Bullmore ET, Brammer MJ, Campbell R, Williams SC, McGuire PK, David AS (1997) Activation of auditory cortex during silent lipreading. Science 276(5312):593–596

    Article  CAS  PubMed  Google Scholar 

  • Choi I, Lee JY, Lee SH (2018) Bottom-up and top-down modulation of multisensory integration. Curr Opin Neurobiol 52:115–122

    Article  CAS  PubMed  Google Scholar 

  • Di Russo F, Berchicci M, Bozzacchi C, Perri RL, Pitzalis S, Spinelli D (2017) Beyond the “Bereitschaftspotential”: action preparation behind cognitive functions. Neurosci Biobehav Rev 78:57–81

    Article  PubMed  Google Scholar 

  • Di Russo F, Berchicci M, Bianco V, Perri RL, Pitzalis S, Quinzi F, Spinelli D (2019) Normative event-related potentials from sensory and cognitive tasks reveal occipital and frontal activities prior and following visual events. Neuroimage 196:173–187

    Article  PubMed  Google Scholar 

  • Faul F, Erdfelder E, Lang AG, Buchner A (2007) G* Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39(2):175–191

    Article  PubMed  Google Scholar 

  • Feldman JI, Dunham K, Cassidy M, Wallace MT, Liu Y, Woynaroski TG (2018) Audiovisual multisensory integration in individuals with autism spectrum disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 95:220–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Fiorini L, Berchicci M, Mussini E, Bianco V, Lucia S, Di Russo F (2021) Neural basis of anticipatory multisensory integration. Brain Sci 11(7):843

    Article  PubMed  PubMed Central  Google Scholar 

  • Fiorini, L., Di Russo, F., Lucia, L., Bianco, V. (2022). Modality predictability modulation confirms the sensorial readiness function of the pre-stimulus activity in sensory brain areas. Cortex, in press.

  • Foxe JJ, Morocz IA, Murray MM, Higgins BA, Javitt DC, Schroeder CE (2000) Multisensory auditory–somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Cogn Brain Res 10:77–83

    Article  CAS  Google Scholar 

  • Friston, K. (2005) A theory of cortical responses. Philosophical Transactions of the Royal Society of London. B Biological Sciences, 360 (1456) 815–836.

  • Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11(5):473–490

    Article  CAS  PubMed  Google Scholar 

  • Macaluso E (2006) Multisensory processing in sensory-specific cortical areas. Neuroscientist 12(4):327–338

    Article  PubMed  Google Scholar 

  • Laurienti PJ et al (2003) Cross-modal sensory processing in the anterior cingulate and medial prefrontal cortices. Hum Brain Mapp 19:213–223

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Seger C, Chen Q, Mo L (2020) Left inferior frontal gyrus integrates multisensory information in category learning. Cereb Cortex 30(8):4410–4423

    Article  PubMed  Google Scholar 

  • Luck SJ, Gaspelin N (2017) How to get statistically significant effects in any ERP experiment (and why you shouldn’t). Psychophysiology 54:146–157

    Article  PubMed  PubMed Central  Google Scholar 

  • Mangun GR, Buck LA (1998) Sustained visual-spatial attention produces costs and benefits in response time and evoked neural activity. Neuropsychologia 36(3):189–200

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Sanchis S (2014) Neurobiological foundations of multisensory integration in people with autism spectrum disorders: the role of the medial prefrontal cortex. Front Hum Neurosci 8:970

    PubMed  PubMed Central  Google Scholar 

  • Matusz PJ, Eimer M (2013) Top-down control of audiovisual search by bimodal search templates. Psychophysiology 50(10):996–1009

    Article  PubMed  Google Scholar 

  • Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ (2002) Multisensory auditory–visual interactions during early sensory processing in humans: a high-density electrical mapping study. Cogn Brain Res 14(1):115–128

    Article  Google Scholar 

  • Morís Fernández L, Macaluso E, Soto-Faraco S (2017) Audiovisual integration as conflict resolution: the conflict of the McGurk illusion. Hum Brain Mapp 38:5691–5705

    Article  PubMed  PubMed Central  Google Scholar 

  • Mussini E, Berchicci M, Bianco V, Perri RL, Quinzi F, Di Russo F (2021) Effect of task complexity on motor and cognitive preparatory brain activities. Int J Psychophysiol 159:11–16

    Article  CAS  PubMed  Google Scholar 

  • Quinzi F, Berchicci M, Bianco V, Perri RL, Di Russo F (2019) The independency of the Bereitschaftspotential from previous stimulus-locked P3 in visuomotor response tasks. Psychophysiology 56(3):e13296

    Article  PubMed  Google Scholar 

  • Ramkhalawansingh R, Keshavarz B, Haycock B, Shahab S, Campos JL (2016) Age differences in visual-auditory self-motion perception during a simulated driving task. Front Psychol 7:595

    Article  PubMed  PubMed Central  Google Scholar 

  • Romanski LM, Hwang J (2012) Timing of audiovisual inputs to the prefrontal cortex and multisensory integration. Neuroscience 214:36–48

    Article  CAS  PubMed  Google Scholar 

  • Salmaso D, Longoni AM (1985) Problems in the assessment of hand preference. Cortex 21(4):533–549

    Article  CAS  PubMed  Google Scholar 

  • Santangelo V, Van der Lubbe RHJ, Belardinelli MO, Postma A (2008) Multisensory integration affects ERP components elicited by exogenous cues. Exp Brain Res 185(2):269–277

    Article  PubMed  Google Scholar 

  • Scheliga S, Kellermann T, Lampert A, Rolke R, Spehr M, Habel U (2022) Neural correlates of multisensory integration in the human brain: an ALE meta-analysis. Rev Neurosci. https://doi.org/10.1515/revneuro-2022-0065

    Article  PubMed  Google Scholar 

  • Spence C, Shore DI, Klein RM (2001) Multisensory prior entry. J Exp Psychol 130:799

    Article  CAS  Google Scholar 

  • Stephen JM, Knoefel JE, Adair J, Hart B, Aine CJ (2010) Aging-related changes in auditory and visual integration measured with MEG. Neurosci Lett 484:76–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson RA, Ghose D, Fister JK, Sarko DK, Altieri NA, Nidiffer AR, Wallace MT (2014) Identifying and quantifying multisensory integration: a tutorial review. Brain Topogr 27(6):707–730

    Article  PubMed  Google Scholar 

  • Talsma D, Senkowski D, Soto-Faraco S, Woldorff MG (2010) The multifaceted interplay between attention and multisensory integration. Trends Cogn Sci 14(9):400–410

    Article  PubMed  PubMed Central  Google Scholar 

  • Talsma D, Woldorff MG (2005) Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J Cogn Neurosci 17:1098–1114

    Article  PubMed  Google Scholar 

  • Tang X, Wu J, Shen Y (2016) The interactions of multisensory integration with endogenous and exogenous attention. Neurosci Biobehav Rev 61:208–224

    Article  PubMed  Google Scholar 

  • Teder-Sälejärvi WA, Di Russo F, McDonald JJ, Hillyard SA (2005) Effects of spatial congruity on audio-visual multimodal integration. J Cogn Neurosci 17(9):1396–1409

    Article  PubMed  Google Scholar 

  • Teder-Sälejärvi WA, McDonald JJ, Di Russo F, Hillyard SA (2002) An analysis of audio-visual crossmodal integration by means of event-related potential (ERP) recordings. Cogn Brain Res 14(1):106–114

    Article  Google Scholar 

  • Van Atteveldt N, Murray MM, Thut G, Schroeder CE (2014) Multisensory integration: flexible use of general operations. Neuron 81(6):1240–1253

    Article  PubMed  PubMed Central  Google Scholar 

  • Visalli A, Capizzi M, Ambrosini E, Kopp B, Vallesi A (2021) Electroencephalographic correlates of temporal Bayesian belief updating and surprise. Neuroimage 231:117867

    Article  PubMed  Google Scholar 

  • Wassenhove VV, Grant KW, Poeppel D, Halle M (2005) Visual speech speeds up the neural processing of auditory speech. Proc Natl Acad Sci USA 102:1181–1186

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams LE, Light GA, Braff DL, Ramachandran VS (2010) Reduced multisensory integration in patients with schizophrenia on a target detection task. Neuropsychologia 48:3128–3136

    Article  PubMed  PubMed Central  Google Scholar 

  • Zikopoulos B, Barbas H (2007) Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18(6):417–438

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the University of Rome “Foro Italico” grant CDR2.BANDO2020DRF to FDR.

Author information

Authors and Affiliations

Authors

Contributions

FDR and VB conceptualized and designed the study. Material preparation, data collection, and analysis were performed by SL, LF, and EM. The first draft of the manuscript was written by SL and FDR and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Stefania Lucia.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lucia, S., Aydin, M., Bianco, V. et al. Effect of anticipatory multisensory integration on sensory–motor performance. Brain Struct Funct 229, 549–559 (2024). https://doi.org/10.1007/s00429-023-02620-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-023-02620-3

Keywords

Navigation