Reciprocal Interactions Between Audition and Touch in Flutter Frequency Perception

In: Multisensory Research

Abstract

In both audition and touch, sensory cues comprising repeating events are perceived either as a continuous signal or as a stream of temporally discrete events (flutter), depending on the events’ repetition rate. At high repetition rates (>100 Hz), auditory and tactile cues interact reciprocally in pitch processing. The frequency of a cue experienced in one modality systematically biases the perceived frequency of a cue experienced in the other modality. Here, we tested whether audition and touch also interact in the processing of low-frequency stimulation. We also tested whether multisensory interactions occurred if the stimulation in one modality comprised click trains and the stimulation in the other modality comprised amplitude-modulated signals. We found that auditory cues bias touch and tactile cues bias audition on a flutter discrimination task. Even though participants were instructed to attend to a single sensory modality and ignore the other cue, the flutter rate in the attended modality is perceived to be similar to that of the distractor modality. Moreover, we observed similar interaction patterns regardless of stimulus type and whether the same stimulus types were experienced by both senses. Combined with earlier studies, our results suggest that the nervous system extracts and combines temporal rate information from multisensory environmental signals, regardless of stimulus type, in both the low- and high temporal frequency domains. This function likely reflects the importance of temporal frequency as a fundamental feature of our multisensory experience.

  • BaddeS.ThomaschewskiL.StoffregenH. and RoderB. (2016). Adapting to Visual and Auditory Low Frequency Modulated Stimuli Induced Enhanced Tactile Frequency Discrimination. Society for NeuroscienceSan Diego, CA, USA.

    • Search Google Scholar
    • Export Citation
  • BendorD. and WangX. (2007). Differential neural coding of acoustic flutter within primate auditory cortexNat. Neurosci. 10763771.

    • Search Google Scholar
    • Export Citation
  • BesserG. M. (1967). Some physiological characteristics of auditory flutter fusion in manNature 2141719.

  • BologniniN.CecchettoC.GeraciC.MaravitaA.Pascual-LeoneA. and PapagnoC. (2011). Hearing shapes our perception of time: temporal discrimination of tactile stimuli in deaf peopleJ. Cogn. Neurosci. 24276286.

    • Search Google Scholar
    • Export Citation
  • BrescianiJ. P. and ErnstM. O. (2007). Signal reliability modulates auditory-tactile integration for event countingNeuroreport 1811571161.

    • Search Google Scholar
    • Export Citation
  • BrescianiJ. P.ErnstM. O.DrewingK.BouyerG.MauryV. and KheddarA. (2005). Feeling what you hear: auditory signals can modulate tactile tap perceptionExp. Brain Res. 162172180.

    • Search Google Scholar
    • Export Citation
  • ConventoS.RahmanM. S. and YauJ. M. (2018). Selective attention gates the interactive crossmodal coupling between perceptual systemsCurr. Biol. 28746752.

    • Search Google Scholar
    • Export Citation
  • CrommettL. E.Perez-BellidoA. and YauJ. M. (2017). Auditory adaptation improves tactile frequency perceptionJ. Neurophysiol. 11713521362.

    • Search Google Scholar
    • Export Citation
  • DrullmanR.FestenJ. M. and PlompR. (1994). Effect of reducing slow temporal modulations on speech receptionJ. Acoust. Soc. Am. 9526702680.

    • Search Google Scholar
    • Export Citation
  • EggermontJ. J. (1993). Differential effects of age on click-rate and amplitude modulation-frequency coding in primary auditory cortex of the catHear. Res. 65175192.

    • Search Google Scholar
    • Export Citation
  • ErnstM. O. and BanksM. S. (2002). Humans integrate visual and haptic information in a statistically optimal fashionNature 415429433.

    • Search Google Scholar
    • Export Citation
  • FoxeJ. J.WylieG. R.MartinezA.SchroederC. E.JavittD. C.GuilfoyleD.RitterW. and MurrayM. M. (2002). Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI studyJ. Neurophysiol. 88540543.

    • Search Google Scholar
    • Export Citation
  • GebhardJ. W. and MowbrayG. (1959). On discriminating the rate of visual flicker and auditory flutterAm. J. Psychol. 72521529.

    • Search Google Scholar
    • Export Citation
  • HaegensS.VergaraJ.Rossi-PoolR.LemusL. and RomoR. (2017). Beta oscillations reflect supramodal information during perceptual judgmentProc. Natl Acad. Sci. USA 1141381013815.

    • Search Google Scholar
    • Export Citation
  • JousmäkiV. and HariR. (1998). Parchment-skin illusion: sound-biased touchCurr. Biol. 8R190.

  • KayserC.PetkovC. I.AugathM. and LogothetisN. K. (2005). Integration of touch and sound in auditory cortexNeuron 48373384.

    • Search Google Scholar
    • Export Citation
  • KleinerM.BrainardD.PelliD.InglingA.MurrayR. and BroussardC. (2007). What’s new in psychtoolbox-3Perception 36116.

    • Search Google Scholar
    • Export Citation
  • KrumbholzK.PattersonR. D. and PressnitzerD. (2000). The lower limit of pitch as determined by rate discriminationJ. Acoust. Soc. Am. 10811701180.

    • Search Google Scholar
    • Export Citation
  • LattnerS.MeyerM. E. and FriedericiA. D. (2005). Voice perception: sex, pitch, and the right hemisphereHum. Brain Mapp. 241120.

    • Search Google Scholar
    • Export Citation
  • LemusL.HernandezA. and RomoR. (2009a). Neural encoding of auditory discrimination in ventral premotor cortexProc. Natl Acad. Sci. USA 1061464014645.

    • Search Google Scholar
    • Export Citation
  • LemusL.HernándezA. and RomoR. (2009b). Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortexProc. Natl Acad. Sci. USA 10694719476.

    • Search Google Scholar
    • Export Citation
  • LemusL.HernandezA.LunaR.ZainosA. and RomoR. (2010). Do sensory cortices process more than one sensory modality during perceptual judgments?Neuron 67335348.

    • Search Google Scholar
    • Export Citation
  • LevitanC. A.BanY. H.StilesN. R. and ShimojoS. (2015). Rate perception adapts across the senses: evidence for a unified timing mechanismSci. Rep. 58857. DOI:10.1038/srep08857.

    • Search Google Scholar
    • Export Citation
  • LiangL.LuT. and WangX. (2002). Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primatesJ. Neurophysiol. 8722372261.

    • Search Google Scholar
    • Export Citation
  • LunghiC.MorroneM. C. and AlaisD. (2014). Auditory and tactile signals combine to influence vision during binocular rivalryJ. Neurosci. 34784792.

    • Search Google Scholar
    • Export Citation
  • MaW. J. and PougetA. (2008). Linking neurons to behavior in multisensory perception: a computational reviewBrain Res. 1242412.

    • Search Google Scholar
    • Export Citation
  • ManfrediL. R.SaalH. P.BrownK. J.ZielinskiM. C.DammannJ. F. 3rdPolashockV. S. and BensmaiaS. J. (2014). Natural scenes in tactile textureJ. Neurophysiol. 11117921802.

    • Search Google Scholar
    • Export Citation
  • MountcastleV. B.TalbotW. H.SakataH. and HyvärinenJ. (1969). Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discriminationJ. Neurophysiol. 32452484.

    • Search Google Scholar
    • Export Citation
  • MountcastleV. B.SteinmetzM. A. and RomoR. (1990). Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeysJ. Neurosci. 1030323044.

    • Search Google Scholar
    • Export Citation
  • NordmarkP. F.PruszynskiJ. A. and JohanssonR. S. (2012). BOLD responses to tactile stimuli in visual and auditory cortex depend on the frequency content of stimulationJ. Cogn. Neurosci. 2421202134.

    • Search Google Scholar
    • Export Citation
  • OccelliV.SpenceC. and ZampiniM. (2011). Audio-tactile interactions in temporal perceptionPsychon. Bull. Rev. 18429454.

  • Pérez-BellidoA.BarnesK. A.CrommettL. E. and YauJ. M. (2017). Auditory frequency representations in human somatosensory cortexCereb. Cortex 2839083921.

    • Search Google Scholar
    • Export Citation
  • RecanzoneG. H. (2003). Auditory influences on visual temporal rate perceptionJ. Neurophysiol. 8910781093.

  • RoT.HsuJ.YasarN. E.ElmoreL. C. and BeauchampM. S. (2009). Sound enhances touch perceptionExp. Brain Res. 195135143.

    • Search Google Scholar
    • Export Citation
  • RoachN. W.HeronJ. and McGrawP. V. (2006). Resolving multisensory conflict: a strategy for balancing the costs and benefits of audio-visual integrationProc. Biol. Sci. 27321592168.

    • Search Google Scholar
    • Export Citation
  • RomoR. and SalinasE. (2003). Flutter discrimination: neural codes, perception, memory and decision makingNat. Rev. Neurosci. 4203218.

    • Search Google Scholar
    • Export Citation
  • SaalH. P.WangX. and BensmaiaS. J. (2016). Importance of spike timing in touch: an analogy with hearing?Curr. Opin. Neurobiol. 40142149.

    • Search Google Scholar
    • Export Citation
  • SchreinerC. E. and UrbasJ. V. (1988). Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fieldsHear. Res. 324963.

    • Search Google Scholar
    • Export Citation
  • SchurmannM.CaetanoG.HlushchukY.JousmakiV. and HariR. (2006). Touch activates human auditory cortexNeuroimage 3013251331.

    • Search Google Scholar
    • Export Citation
  • ShamsL. and BeierholmU. R. (2010). Causal inference in perceptionTrends Cogn. Sci. 14425432.

  • ShipleyT. (1964). Auditory flutter-driving of visual flickerScience 14513281330.

  • TalbotW. H.Darian-SmithI.KornhuberH. H. and MountcastleV. B. (1968). The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey handJ. Neurophysiol. 31301334.

    • Search Google Scholar
    • Export Citation
  • VergaraJ.RiveraN.Rossi-PoolR. and RomoR. (2016). A neural parametric code for storing information of more than one sensory modality in working memoryNeuron 895462.

    • Search Google Scholar
    • Export Citation
  • WelchR. B.DutionHurtL. D. and WarrenD. H. (1986). Contributions of audition and vision to temporal rate perceptionPercept. Psychophys. 39294300.

    • Search Google Scholar
    • Export Citation
  • WilsonE. C.ReedC. M. and BraidaL. D. (2010). Integration of auditory and vibrotactile stimuli: effects of frequencyJ. Acoust. Soc. Am. 12730443059.

    • Search Google Scholar
    • Export Citation
  • WoznyD. R.BeierholmU. R. and ShamsL. (2008). Human trimodal perception follows optimal statistical inferenceJ. Vis. 8111.

    • Search Google Scholar
    • Export Citation
  • YauJ. M.OlenczakJ. B.DammannJ. F. and BensmaiaS. J. (2009a). Temporal frequency channels are linked across audition and touchCurr. Biol. 19561566.

    • Search Google Scholar
    • Export Citation
  • YauJ. M.HollinsM. and BensmaiaS. J. (2009b). Textural timbre: the perception of surface microtexture depends in part on multimodal spectral cuesCommun. Integr. Biol. 2344346.

    • Search Google Scholar
    • Export Citation
  • YauJ. M.WeberA. I. and BensmaiaS. J. (2010). Separate mechanisms for audio-tactile pitch and loudness interactionsFront. Psychol. 1160. DOI:10.3389/fpsyg.2010.00160.

    • Search Google Scholar
    • Export Citation
  • YauJ. M.CelnikP.HsiaoS. S. and DesmondJ. E. (2014). Feeling better: separate pathways for targeted enhancement of spatial and temporal touchPsychol. Sci. 25555565.

    • Search Google Scholar
    • Export Citation
  • YauJ. M.DeAngelisG. C. and AngelakiD. E. (2015). Dissecting neural circuits for multisensory integration and crossmodal processingPhilos. Trans. R. Soc. Lond. B Biol. Sci. 37020140203. DOI:10.1098/rstb.2014.0203.

    • Search Google Scholar
    • Export Citation

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 400 294 17
Full Text Views 40 19 0
PDF Downloads 18 10 0