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Modality-specific sensory readiness for upcoming events revealed by slow cortical potentials

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Abstract

Human brain activity allows to anticipate future events and to prepare the next action accordingly; consistently, event-related potential (ERP) studies found action preparatory brain activities in the premotor and prefrontal cortex. In the present study, we investigated the preparatory activity in the sensory cortical regions. Slow cortical potentials were recorded during passive tasks, i.e., subjects expected for a sensory stimulus and no motor or cognitive response were required. In particular, we tested the hypothesis that perceptual anticipatory cortical mechanisms were modality specific. Three groups of 21 young adults underwent passive perceptual tasks in different sensory modalities (visual, auditory, or somatosensory). We confirmed the presence of a visual negativity (vN) component for the visual modality starting about 800 ms before stimulus with source in extrastriate areas and we found novel modality-specific sensory readiness components for the auditory and somatosensory modalities. The auditory positivity (aP) started about 800 ms before stimulus with source in bilateral auditory cortices and the somatosensory negativity (sN) started about 500 ms before stimulus with source in the somatosensory secondary cortex, contralateral to the stimulated hand. The scalp topography and intracranial sources of these three slow preparatory activities were mirrored with inverted polarity at early post-stimulus stage evoking the well-known visual P1, auditory N1, and somatosensory P100 components. Present findings contribute to widening the family of slow wave preparatory components, providing evidence about the relationship between top–down and bottom–up processing in sensory perception.

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References

  • Bastiaansen MC, Böcker KB, Brunia CH, De Munck JC, Spekreijse H (2001) Event-related desynchronization during anticipatory attention for an upcoming stimulus: a comparative EEG/MEG study. Clin Neurophysiol 112(2):393–403

    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

    CAS  PubMed  Google Scholar 

  • Binder JR, Rao SM, Hammeke TA, Yetkin FZ, Jesmanowicz A, Bandettini PA, Hyde JS (1994) Functional magnetic resonance imaging of human auditory cortex. Ann Neurol 35(6):662–672

    CAS  PubMed  Google Scholar 

  • Birbaumer N, Elbert T, Canavan AG, Rockstroh B (1990) Slow potentials of the cerebral cortex and behavior. Physiol Rev 70(1):1–41

    CAS  PubMed  Google Scholar 

  • Blakemore SJ, Goodbody SJ, Wolpert DM (1998) Predicting the consequences of our own actions: the role of sensorimotor context estimation. J Neurosci 18(18):7511–7518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt ME, Jansen BH (1991) The relationship between prestimulus alpha amplitude and visual evoked potential amplitude. Int J Neurosci 61(3–4):261–268

    CAS  PubMed  Google Scholar 

  • Brunia CH (1993) Waiting in readiness: gating in attention and motor preparation. Psychophysiology 30(4):327–339

    CAS  PubMed  Google Scholar 

  • Damen EJP, Brunia CHM (1985) Slow brain potentials related to movement and visual feedback in a response timing task. Biol Psychol 20(3):195

    Google Scholar 

  • de Lange FP, Heilbron M, Kok P (2018) How do expectations shape perception? Trends Cogn Sci 22(9):764–779

    PubMed  Google Scholar 

  • Desmedt JE, Robertson D (1977) Differential enhancement of early and late components of the cerebral somatosensory evoked potentials during forced-paced cognitive tasks in man. J Physiol 271(3):761–782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Di Russo F, Pitzalis S (2013) EEG-fMRI combination for the study of visual perception and spatial attention. Cognitive electrophysiology of attention: signals of the mind. Academic Press, New York, pp 58–70

    Google Scholar 

  • Di Russo F, Lucci G, Sulpizio V, Berchicci M, Spinelli D, Pitzalis S, Galati G (2016) Spatiotemporal brain mapping during preparation, perception, and action. NeuroImage 126:1–14

    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

    PubMed  Google Scholar 

  • Dionne JK, Meehan SK, Legon W, Staines WR (2010) Crossmodal influences in somatosensory cortex: interaction of vision and touch. Hum Brain Mapp 31(1):14–25

    PubMed  Google Scholar 

  • Fellinger R, Klimesch W, Gruber W, Freunberger R, Doppelmayr M (2011) Pre-stimulus alpha phase-alignment predicts P1-amplitude. Brain Res Bull 85(6):417–423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ford JM, Palzes VA, Roach BJ, Mathalon DH (2013) Did I do that? Abnormal predictive processes in schizophrenia when button pressing to deliver a tone. Schizophr Bull 40(4):804–812

    PubMed  PubMed Central  Google Scholar 

  • Friston K (2005) A theory of cortical responses. Philos Trans R Soc Lond Biol Sci 360(1456):815–836

    Google Scholar 

  • Fu KMG, Foxe JJ, Murray MM, Higgins BA, Javitt DC, Schroeder CE (2001) Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations. Cogn Brain Res 12(1):145–152

    CAS  Google Scholar 

  • Goff GD, Matsumiya Y, Allison T, Goff WR (1977) The scalp topography of human somatosensory and auditory evoked potentials. Electroencephalogr Clin Neurophysiol 42(1):57–76

    CAS  PubMed  Google Scholar 

  • Gomez CM, Marco J, Grau C (2003) Preparatory visuo-motor cortical network of the contingent negative variation estimated by current density. Neuroimage 20(1):216–224

    CAS  PubMed  Google Scholar 

  • Grady CL, Van Meter JW, Maisog JM, Pietrini P, Krasuski J, Rauschecker JP (1997) Attention-related modulation of activity in primary and secondary auditory cortex. NeuroReport 8(11):2511–2516

    CAS  PubMed  Google Scholar 

  • Handy TC (ed) (2005) Event-related potentials: a methods handbook. MIT press, Cambridge

    Google Scholar 

  • Hari R, Karhu J, Hämäläinen M, Knuutila J, Salonen O, Sams M, Vilkman V (1993) Functional organization of the human first and second somatosensory cortices: a neuromagnetic study. Eur J Neurosci 5(6):724–734

    CAS  PubMed  Google Scholar 

  • Hillyard SA, Anllo-Vento L (1998) Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci 95(3):781–787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes G, Waszak F (2011) ERP correlates of action effect prediction and visual sensory attenuation in voluntary action. Neuroimage 56(3):1632–1640

    PubMed  Google Scholar 

  • Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements: I An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118(4):913–933

    PubMed  Google Scholar 

  • Kakigi R (1986) Ipsilateral and contralateral SEP components following median nerve stimulation: effects of interfering stimuli applied to the contralateral hand. Electroencephalogr Clin Neurophysiol 64(3):246–259

    CAS  PubMed  Google Scholar 

  • Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22(4):751–761

    CAS  PubMed  Google Scholar 

  • Key APF, Dove GO, Maguire MJ (2005) Linking brainwaves to the brain: an ERP primer. Dev Neuropsychol 27(2):183–215

    PubMed  Google Scholar 

  • Knill DC, Richards W (eds) (1996) Perception as Bayesian inference. Cambridge University Press

  • Kornhuber HH, Deecke L (1965) Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: bereitschaftspotential und reafferente Potentiale. Pflüger’s Archiv für die gesamte Physiologie des Menschen und der Tiere 284(1):1–17

    CAS  Google Scholar 

  • Kotani Y, Ohgami Y, Yoshida N, Kiryu S, Inoue Y (2017) Anticipation process of the human brain measured by stimulus-preceding negativity (SPN). J Phys Fit Sports Med 6(1):7–14

    Google Scholar 

  • Kutas M, Donchin E (1980) Preparation to respond as manifested by movement-related brain potentials. Brain Res 202(1):95–115

    CAS  PubMed  Google Scholar 

  • Langner R, Kellermann T, Boers F, Sturm W, Willmes K, Eickhoff SB (2011) Modality-specific perceptual expectations selectively modulate baseline activity in auditory, somatosensory, and visual cortices. Cereb Cortex 21(12):2850–2862

    PubMed  Google Scholar 

  • Larrea LG, Bastuji H, Mauguière F (1992) Unmasking of cortical SEP components by changes in stimulus rate: a topographic study. Electroencephalogr Clin Neurophysiol Evoked Potentials Sect 84(1):71–83

    Google Scholar 

  • Lawrence SJ, Formisano E, Muckli L, de Lange FP (2017) Laminar fMRI: applications for cognitive neuroscience. Neuroimage 197:785–791

    PubMed  Google Scholar 

  • Lehmann C, Herdener M, Esposito F, Hubl D, Di Salle F, Scheffler K, Seifritz E (2006) Differential patterns of multisensory interactions in core and belt areas of human auditory cortex. Neuroimage 31(1):294–300

    PubMed  Google Scholar 

  • Liu Y, Bengson J, Huang H, Mangun GR, Ding M (2014) Top-down modulation of neural activity in anticipatory visual attention: control mechanisms revealed by simultaneous EEG-fMRI. Cereb Cortex 26(2):517–529

    PubMed  PubMed Central  Google Scholar 

  • Mamassian P, Landy M, Maloney LT (2002) Bayesian modelling of visual perception. Probabilistic models of the brain. MIT Press, Cambridge, pp 13–36

    Google Scholar 

  • Nunez PL, Srinivasan R (2006) Electric fields of the brain: the neurophysics of EEG. Oxford University Press, USA

    Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychol 9(1):97–113

    CAS  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. Psychophysiol 56(3):e13296

    Google Scholar 

  • Rao RP, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2(1):79

    CAS  PubMed  Google Scholar 

  • Reznik D, Simon S, Mukamel R (2018) Predicted sensory consequences of voluntary actions modulate amplitude of preceding readiness potentials. Neuropsychologia 119:302–307

    PubMed  Google Scholar 

  • Rockstroh B (1989) Slow cortical potentials and behaviour. Urban & Schwarzenberg

  • Romei V, Gross J, Thut G (2010) On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J Neurosci 30(25):8692–8697

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanmiguel I, Todd J, Schröger E (2013) Sensory suppression effects to self-initiated sounds reflect the attenuation of the unspecific N1 component of the auditory ERP. Psychophysiology 50(4):334–343

    PubMed  Google Scholar 

  • Sauseng P, Klimesch W, Stadler W, Schabus M, Doppelmayr M, Hanslmayr S, Birbaumer N (2005) A shift of visual spatial attention is selectively associated with human EEG alpha activity. Eur J Neurosci 22(11):2917–2926

    CAS  PubMed  Google Scholar 

  • Schürmann M, Caetano G, Hlushchuk Y, Jousmäki V, Hari R (2006) Touch activates human auditory cortex. Neuroimage 30(4):1325–1331

    PubMed  Google Scholar 

  • Shin YK, Proctor RW, Capaldi EJ (2010) A review of contemporary ideomotor theory. Psychol Bull 136(6):943

    PubMed  Google Scholar 

  • Simpson GV, Weber DL, Dale CL, Pantazis D, Bressler SL, Leahy RM, Luks TL (2011) Dynamic activation of frontal, parietal, and sensory regions underlying anticipatory visual spatial attention. J Neurosci 31(39):13880–13889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skinner JE, Yingling CD (1976) Regulation of slow potential shifts in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. Electroencephalogr Clin Neurophysiol 40(3):288–296

    CAS  PubMed  Google Scholar 

  • Staines WR, Popovich C, Legon JK, Adams MS (2014) Early modality-specific somatosensory cortical regions are modulated by attended visual stimuli: interaction of vision, touch and behavioral intent. Front Psychol 5:351

    PubMed  PubMed Central  Google Scholar 

  • Van Boxtel GJ, Böcker KB (2004) Cortical measures of anticipation. J Psychophysiol 18(2/3):61–76

    Google Scholar 

  • Van Dijk H, Schoffelen JM, Oostenveld R, Jensen O (2008) Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 28(8):1816–1823

    PubMed  PubMed Central  Google Scholar 

  • Vercillo T, O’Neil S, Jiang F (2018) Action-effect contingency modulates the readiness potential. NeuroImage 183:273–279

    PubMed  Google Scholar 

  • Zouridakis G, Simos PG, Papanicolaou AC (1998) Multiple bilaterally asymmetric cortical sources account for the auditory N1 m component. Brain Topogr 10(3):183–189

    CAS  PubMed  Google Scholar 

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Acknowledgements

The study was supported by the University of Rome “Foro Italico” and Santa Lucia Foundation.

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Correspondence to V. Bianco.

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Bianco, V., Perri, R.L., Berchicci, M. et al. Modality-specific sensory readiness for upcoming events revealed by slow cortical potentials. Brain Struct Funct 225, 149–159 (2020). https://doi.org/10.1007/s00429-019-01993-8

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