Skip to main content
Erschienen in: Brain Structure and Function 3/2024

21.02.2023 | Original Article

Effect of anticipatory multisensory integration on sensory–motor performance

verfasst von: Stefania Lucia, Merve Aydin, Valentina Bianco, Linda Fiorini, Elena Mussini, Francesco Di Russo

Erschienen in: Brain Structure and Function | Ausgabe 3/2024

Einloggen, um Zugang zu erhalten

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.
Literatur
Zurück zum Zitat Beauchamp MS, Lee KE, Argall BD, Martin A (2004) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823PubMedCrossRef Beauchamp MS, Lee KE, Argall BD, Martin A (2004) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823PubMedCrossRef
Zurück zum Zitat Berchicci M, Lucci G, Pesce C, Spinelli D, Di Russo F (2012) Prefrontal hyperactivity in older people during motor planning. Neuroimage 62(3):1750–1760PubMedCrossRef Berchicci M, Lucci G, Pesce C, Spinelli D, Di Russo F (2012) Prefrontal hyperactivity in older people during motor planning. Neuroimage 62(3):1750–1760PubMedCrossRef
Zurück zum Zitat 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 298:211–219PubMedCrossRef 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 298:211–219PubMedCrossRef
Zurück zum Zitat 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 117:202–215PubMedCrossRef 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 117:202–215PubMedCrossRef
Zurück zum Zitat 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):e13369PubMedCrossRef 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):e13369PubMedCrossRef
Zurück zum Zitat 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):149–159PubMedCrossRef 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):149–159PubMedCrossRef
Zurück zum Zitat 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):e13687PubMedCrossRef 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):e13687PubMedCrossRef
Zurück zum Zitat 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):18751–18756PubMedPubMedCentralCrossRef 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):18751–18756PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):593–596PubMedCrossRef 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):593–596PubMedCrossRef
Zurück zum Zitat Choi I, Lee JY, Lee SH (2018) Bottom-up and top-down modulation of multisensory integration. Curr Opin Neurobiol 52:115–122PubMedCrossRef Choi I, Lee JY, Lee SH (2018) Bottom-up and top-down modulation of multisensory integration. Curr Opin Neurobiol 52:115–122PubMedCrossRef
Zurück zum Zitat 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 78:57–81PubMedCrossRef 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 78:57–81PubMedCrossRef
Zurück zum Zitat 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 196:173–187PubMedCrossRef 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 196:173–187PubMedCrossRef
Zurück zum Zitat 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):175–191PubMedCrossRef 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):175–191PubMedCrossRef
Zurück zum Zitat 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 95:220–234PubMedPubMedCentralCrossRef 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 95:220–234PubMedPubMedCentralCrossRef
Zurück zum Zitat Fiorini L, Berchicci M, Mussini E, Bianco V, Lucia S, Di Russo F (2021) Neural basis of anticipatory multisensory integration. Brain Sci 11(7):843PubMedPubMedCentralCrossRef Fiorini L, Berchicci M, Mussini E, Bianco V, Lucia S, Di Russo F (2021) Neural basis of anticipatory multisensory integration. Brain Sci 11(7):843PubMedPubMedCentralCrossRef
Zurück zum Zitat 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. 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.
Zurück zum Zitat 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 10:77–83CrossRef 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 10:77–83CrossRef
Zurück zum Zitat Friston, K. (2005) A theory of cortical responses. Philosophical Transactions of the Royal Society of London. B Biological Sciences, 360 (1456) 815–836. Friston, K. (2005) A theory of cortical responses. Philosophical Transactions of the Royal Society of London. B Biological Sciences, 360 (1456) 815–836.
Zurück zum Zitat Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11(5):473–490PubMedCrossRef Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11(5):473–490PubMedCrossRef
Zurück zum Zitat Macaluso E (2006) Multisensory processing in sensory-specific cortical areas. Neuroscientist 12(4):327–338PubMedCrossRef Macaluso E (2006) Multisensory processing in sensory-specific cortical areas. Neuroscientist 12(4):327–338PubMedCrossRef
Zurück zum Zitat Li Y, Seger C, Chen Q, Mo L (2020) Left inferior frontal gyrus integrates multisensory information in category learning. Cereb Cortex 30(8):4410–4423PubMedCrossRef Li Y, Seger C, Chen Q, Mo L (2020) Left inferior frontal gyrus integrates multisensory information in category learning. Cereb Cortex 30(8):4410–4423PubMedCrossRef
Zurück zum Zitat Luck SJ, Gaspelin N (2017) How to get statistically significant effects in any ERP experiment (and why you shouldn’t). Psychophysiology 54:146–157PubMedPubMedCentralCrossRef Luck SJ, Gaspelin N (2017) How to get statistically significant effects in any ERP experiment (and why you shouldn’t). Psychophysiology 54:146–157PubMedPubMedCentralCrossRef
Zurück zum Zitat Mangun GR, Buck LA (1998) Sustained visual-spatial attention produces costs and benefits in response time and evoked neural activity. Neuropsychologia 36(3):189–200PubMedCrossRef Mangun GR, Buck LA (1998) Sustained visual-spatial attention produces costs and benefits in response time and evoked neural activity. Neuropsychologia 36(3):189–200PubMedCrossRef
Zurück zum Zitat 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 8:970PubMedPubMedCentral 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 8:970PubMedPubMedCentral
Zurück zum Zitat Matusz PJ, Eimer M (2013) Top-down control of audiovisual search by bimodal search templates. Psychophysiology 50(10):996–1009PubMedCrossRef Matusz PJ, Eimer M (2013) Top-down control of audiovisual search by bimodal search templates. Psychophysiology 50(10):996–1009PubMedCrossRef
Zurück zum Zitat 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):115–128CrossRef 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):115–128CrossRef
Zurück zum Zitat Morís Fernández L, Macaluso E, Soto-Faraco S (2017) Audiovisual integration as conflict resolution: the conflict of the McGurk illusion. Hum Brain Mapp 38:5691–5705PubMedPubMedCentralCrossRef Morís Fernández L, Macaluso E, Soto-Faraco S (2017) Audiovisual integration as conflict resolution: the conflict of the McGurk illusion. Hum Brain Mapp 38:5691–5705PubMedPubMedCentralCrossRef
Zurück zum Zitat 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 159:11–16PubMedCrossRef 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 159:11–16PubMedCrossRef
Zurück zum Zitat 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):e13296PubMedCrossRef 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):e13296PubMedCrossRef
Zurück zum Zitat 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 7:595PubMedPubMedCentralCrossRef 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 7:595PubMedPubMedCentralCrossRef
Zurück zum Zitat Romanski LM, Hwang J (2012) Timing of audiovisual inputs to the prefrontal cortex and multisensory integration. Neuroscience 214:36–48PubMedCrossRef Romanski LM, Hwang J (2012) Timing of audiovisual inputs to the prefrontal cortex and multisensory integration. Neuroscience 214:36–48PubMedCrossRef
Zurück zum Zitat Salmaso D, Longoni AM (1985) Problems in the assessment of hand preference. Cortex 21(4):533–549PubMedCrossRef Salmaso D, Longoni AM (1985) Problems in the assessment of hand preference. Cortex 21(4):533–549PubMedCrossRef
Zurück zum Zitat 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):269–277PubMedCrossRef 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):269–277PubMedCrossRef
Zurück zum Zitat Spence C, Shore DI, Klein RM (2001) Multisensory prior entry. J Exp Psychol 130:799CrossRef Spence C, Shore DI, Klein RM (2001) Multisensory prior entry. J Exp Psychol 130:799CrossRef
Zurück zum Zitat Stephen JM, Knoefel JE, Adair J, Hart B, Aine CJ (2010) Aging-related changes in auditory and visual integration measured with MEG. Neurosci Lett 484:76–80PubMedPubMedCentralCrossRef Stephen JM, Knoefel JE, Adair J, Hart B, Aine CJ (2010) Aging-related changes in auditory and visual integration measured with MEG. Neurosci Lett 484:76–80PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):707–730PubMedCrossRef 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):707–730PubMedCrossRef
Zurück zum Zitat Talsma D, Senkowski D, Soto-Faraco S, Woldorff MG (2010) The multifaceted interplay between attention and multisensory integration. Trends Cogn Sci 14(9):400–410PubMedPubMedCentralCrossRef Talsma D, Senkowski D, Soto-Faraco S, Woldorff MG (2010) The multifaceted interplay between attention and multisensory integration. Trends Cogn Sci 14(9):400–410PubMedPubMedCentralCrossRef
Zurück zum Zitat Talsma D, Woldorff MG (2005) Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J Cogn Neurosci 17:1098–1114PubMedCrossRef Talsma D, Woldorff MG (2005) Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J Cogn Neurosci 17:1098–1114PubMedCrossRef
Zurück zum Zitat Tang X, Wu J, Shen Y (2016) The interactions of multisensory integration with endogenous and exogenous attention. Neurosci Biobehav Rev 61:208–224PubMedCrossRef Tang X, Wu J, Shen Y (2016) The interactions of multisensory integration with endogenous and exogenous attention. Neurosci Biobehav Rev 61:208–224PubMedCrossRef
Zurück zum Zitat 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):1396–1409PubMedCrossRef 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):1396–1409PubMedCrossRef
Zurück zum Zitat 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):106–114CrossRef 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):106–114CrossRef
Zurück zum Zitat Visalli A, Capizzi M, Ambrosini E, Kopp B, Vallesi A (2021) Electroencephalographic correlates of temporal Bayesian belief updating and surprise. Neuroimage 231:117867PubMedCrossRef Visalli A, Capizzi M, Ambrosini E, Kopp B, Vallesi A (2021) Electroencephalographic correlates of temporal Bayesian belief updating and surprise. Neuroimage 231:117867PubMedCrossRef
Zurück zum Zitat Wassenhove VV, Grant KW, Poeppel D, Halle M (2005) Visual speech speeds up the neural processing of auditory speech. Proc Natl Acad Sci USA 102:1181–1186PubMedPubMedCentralCrossRef Wassenhove VV, Grant KW, Poeppel D, Halle M (2005) Visual speech speeds up the neural processing of auditory speech. Proc Natl Acad Sci USA 102:1181–1186PubMedPubMedCentralCrossRef
Zurück zum Zitat Williams LE, Light GA, Braff DL, Ramachandran VS (2010) Reduced multisensory integration in patients with schizophrenia on a target detection task. Neuropsychologia 48:3128–3136PubMedPubMedCentralCrossRef Williams LE, Light GA, Braff DL, Ramachandran VS (2010) Reduced multisensory integration in patients with schizophrenia on a target detection task. Neuropsychologia 48:3128–3136PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):417–438PubMedPubMedCentralCrossRef 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):417–438PubMedPubMedCentralCrossRef
Metadaten
Titel
Effect of anticipatory multisensory integration on sensory–motor performance
verfasst von
Stefania Lucia
Merve Aydin
Valentina Bianco
Linda Fiorini
Elena Mussini
Francesco Di Russo
Publikationsdatum
21.02.2023
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 3/2024
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-023-02620-3

Weitere Artikel der Ausgabe 3/2024

Brain Structure and Function 3/2024 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Viertel reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Bluttest erkennt Parkinson schon zehn Jahre vor der Diagnose

10.05.2024 Parkinson-Krankheit Nachrichten

Ein Bluttest kann abnorm aggregiertes Alpha-Synuclein bei einigen Menschen schon zehn Jahre vor Beginn der motorischen Parkinsonsymptome nachweisen. Mit einem solchen Test lassen sich möglicherweise Prodromalstadien erfassen und die Betroffenen früher behandeln.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.