Log in

Brain Dynamics of Distractibility: Interaction Between Top-Down and Bottom-Up Mechanisms of Auditory Attention

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Attention improves the processing of specific information while other stimuli are disregarded. A good balance between bottom-up (attentional capture by unexpected salient stimuli) and top-down (selection of relevant information) mechanisms is crucial to be both task-efficient and aware of our environment. Only few studies have explored how an isolated unexpected task-irrelevant stimulus outside the attention focus can disturb the top-down attention mechanisms necessary to the good performance of the ongoing task, and how these top-down mechanisms can modulate the bottom-up mechanisms of attentional capture triggered by an unexpected event. We recorded scalp electroencephalography in 18 young adults performing a new paradigm measuring distractibility and assessing both bottom-up and top-down attention mechanisms, at the same time. Increasing task load in top-down attention was found to reduce early processing of the distracting sound, but not bottom-up attentional capture mechanisms nor the behavioral distraction cost in reaction time. Moreover, the impact of bottom-up attentional capture by distracting sounds on target processing was revealed as a delayed latency of the N100 sensory response to target sounds mirroring increased reaction times. These results provide crucial information into how bottom-up and top-down mechanisms dynamically interact and compete in the human brain, i.e. on the precarious balance between voluntary attention and distraction.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Aguera PE, Jerbi K, Caclin A, Bertrand O (2011) ELAN: a software package for analysis and visualization of MEG, EEG, and LFP signals. Comput Intell Neurosci 2011:158970. doi:10.1155/2011/158970

    PubMed Central  PubMed  Google Scholar 

  • Alcaini M, Giard MH, Thevenet M, Pernier J (1994) Two separate frontal components in the N1 wave of the human auditory evoked response. Psychophysiology 31(6):611–615

    Article  CAS  PubMed  Google Scholar 

  • Barry RJ, Macdonald B, Rushby JA (2011) Single-trial event-related potentials and the orienting reflex to monaural tones. Int J Psychophysiol 79(2):127–136. doi:10.1016/j.ijpsycho.2010.09.010

    Article  PubMed  Google Scholar 

  • Berti S (2013) The role of auditory transient and deviance processing in distraction of task performance: a combined behavioral and event-related brain potential study. Front Hum Neurosci 7:352. doi:10.3389/fnhum.2013.00352

    Article  PubMed Central  PubMed  Google Scholar 

  • Bidet-Caulet A, Fischer C, Besle J, Aguera PE, Giard MH, Bertrand O (2007) Effects of selective attention on the electrophysiological representation of concurrent sounds in the human auditory cortex. J Neurosci 27(35):9252–9261

    Article  CAS  PubMed  Google Scholar 

  • Bidet-Caulet A, Mikyska C, Knight RT (2010) Load effects in auditory selective attention: evidence for distinct facilitation and inhibition mechanisms. Neuroimage 50(1):277–284. doi:10.1016/j.neuroimage.2009.12.039

    Article  PubMed Central  PubMed  Google Scholar 

  • Brunia CH, van Boxtel GJ (2001) Wait and see. Int J Psychophysiol 43(1):59–75

    Article  CAS  PubMed  Google Scholar 

  • Ceponiene R, Lepisto T, Soininen M, Aronen E, Alku P, Naatanen R (2004) Event-related potentials associated with sound discrimination versus novelty detection in children. Psychophysiology 41(1):130–141. doi:10.1111/j.1469-8986.2003.00138.x

    Article  CAS  PubMed  Google Scholar 

  • Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215

    Article  CAS  PubMed  Google Scholar 

  • Corral MJ, Escera C (2008) Effects of sound location on visual task performance and electrophysiological measures of distraction. NeuroReport 19(15):1535–1539. doi:10.1097/WNR.0b013e3283110416

    Article  PubMed  Google Scholar 

  • Coull JT (1998) Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology. Prog Neurobiol 55(4):343–361

    Article  CAS  PubMed  Google Scholar 

  • Czigler I, Csibra G, Csontos A (1992) Age and inter-stimulus interval effects on event-related potentials to frequent and infrequent auditory stimuli. Biol Psychol 33(2–3):195–206

    Article  CAS  PubMed  Google Scholar 

  • Davis H, Mast T, Yoshie N, Zerlin S (1966) The slow response of the human cortex to auditory stimuli: recovery process. Electroencephalogr Clin Neurophysiol 21:105–113

    Article  CAS  PubMed  Google Scholar 

  • Dominguez-Borras J, Garcia-Garcia M, Escera C (2008) Emotional context enhances auditory novelty processing: behavioural and electrophysiological evidence. Eur J Neurosci 28(6):1199–1206. doi:10.1111/j.1460-9568.2008.06411.x

    Article  PubMed  Google Scholar 

  • Duncan-Johnson CC, Donchin E (1977) On quantifying surprise: the variation of event-related potentials with subjective probability. Psychophysiology 14(5):456–467

    Article  CAS  PubMed  Google Scholar 

  • Edgington ES (1995) Randomization tests: revised and expanded. Statistics: textbooks and monographs, vol 147, 3rd edn. Marcel Dekker, New York

    Google Scholar 

  • Escera C, Alho K, Winkler I, Naatanen R (1998) Neural mechanisms of involuntary attention to acoustic novelty and change. J Cogn Neurosci 10(5):590–604

    Article  CAS  PubMed  Google Scholar 

  • Escera C, Alho K, Schroger E, Winkler I (2000) Involuntary attention and distractibility as evaluated with event-related brain potentials. Audiol Neurootol 5(3–4):151–166

    Article  CAS  PubMed  Google Scholar 

  • Escera C, Yago E, Corral MJ, Corbera S, Nunez MI (2003) Attention capture by auditory significant stimuli: semantic analysis follows attention switching. Eur J Neurosci 18(8):2408–2412

    Article  PubMed  Google Scholar 

  • Escera C, Corral MJ (2007) Role of mismatch negativity and novelty-P3 in involuntary auditory attention. J Psychophysiol 21(3–4):251–264. doi:10.1027/0269-8803.21.34.251

    Article  Google Scholar 

  • Foxe JJ, Snyder AC (2011) The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention. Front Psychol 2:154. doi:10.3389/fpsyg.2011.00154

    Article  PubMed Central  PubMed  Google Scholar 

  • Friedman D, Cycowicz YM, Gaeta H (2001) The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty. Neurosci Biobehav Rev 25(4):355–373

    Article  CAS  PubMed  Google Scholar 

  • Giard MH, Fort A, Mouchetant-Rostaing Y, Pernier J (2000) Neurophysiological mechanisms of auditory selective attention in humans. Front Biosci 5:D84–94

    Article  CAS  PubMed  Google Scholar 

  • Gilley PM, Sharma A, Dorman M, Martin K (2005) Developmental changes in refractoriness of the cortical auditory evoked potential. Clin Neurophysiol 116(3):648–657. doi:10.1016/j.clinph.2004.09.009

    Article  PubMed  Google Scholar 

  • Golob EJ, Pratt H, Starr A (2002) Preparatory slow potentials and event-related potentials in an auditory cued attention task. Clin Neurophysiol 113(10):1544–1557

    Article  CAS  PubMed  Google Scholar 

  • Gomez CM, Flores A, Ledesma A (2007) Fronto-parietal networks activation during the contingent negative variation period. Brain Res Bull 73(1–3):40–47. doi:10.1016/j.brainresbull.2007.01.015

    Article  PubMed  Google Scholar 

  • Hari R, Kaila K, Katila T, Tuomisto T, Varpula T (1982) Interstimulus interval dependence on the auditory vertex response and its magnetic counterpart: implications for their neural generation. Electroencephalogr Clin Neurophysiol 54:561–569

    Article  CAS  PubMed  Google Scholar 

  • Harmony T, Bernal J, Fernandez T, Silva-Pereyra J, Fernandez-Bouzas A, Marosi E, Rodriguez M, Reyes A (2000) Primary task demands modulate P3a amplitude. Brain Res Cogn Brain Res 9(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Hillyard SA, Hink RF, Schwent VL, Picton TW (1973) Electrical signs of selective attention in the human brain. Science 182(108):177–180

    Article  CAS  PubMed  Google Scholar 

  • Holeckova I, Fischer C, Giard MH, Delpuech C, Morlet D (2006) Brain responses to a subject’s own name uttered by a familiar voice. Brain Res 1082(1):142–152

    Article  CAS  PubMed  Google Scholar 

  • Horvath J (2013) Sensory ERP effects in auditory distraction: did we miss the main event? Psychol Res. doi:10.1007/s00426-013-0507-7

    PubMed  Google Scholar 

  • Horvath J, Winkler I, Bendixen A (2008) Do N1/MMN, P3a, and RON form a strongly coupled chain reflecting the three stages of auditory distraction? Biol Psychol 79(2):139–147. doi:10.1016/j.biopsycho.2008.04.001

    Article  PubMed  Google Scholar 

  • Hugdahl K, Nordby H (1994) Electrophysiological correlates to cued attentional shifts in the visual and auditory modalities. Behav Neural Biol 62(1):21–32

    Article  CAS  PubMed  Google Scholar 

  • Imada T, Watanabe M, Mashiko T, Kawakatsu M, Kotani M (1997) The silent period between sounds has a stronger effect than the interstimulus interval on auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 102(1):37–45

    Article  CAS  PubMed  Google Scholar 

  • Jensen O, Mazaheri A (2010) Sha** functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186. doi:10.3389/fnhum.2010.00186

    Article  PubMed Central  PubMed  Google Scholar 

  • Knight R (1996) Contribution of human hippocampal region to novelty detection. Nature 383(6597):256–259. doi:10.1038/383256a0

    Article  CAS  PubMed  Google Scholar 

  • Ljungberg JK, Parmentier FB, Leiva A, Vega N (2012) The informational constraints of behavioral distraction by unexpected sounds: the role of event information. J Exp Psychol Learn Mem Cogn 38(5):1461–1468. doi:10.1037/a0028149

    Article  PubMed  Google Scholar 

  • Lv JY, Wang T, Qiu J, Feng SH, Tu S, Wei DT (2010) The electrophysiological effect of working memory load on involuntary attention in an auditory–visual distraction paradigm: an ERP study. Exp Brain Res 205(1):81–86. doi:10.1007/s00221-010-2360-x

    Article  PubMed  Google Scholar 

  • Lyytinen H, Blomberg AP, Naatanen R (1992) Event-related potentials and autonomic responses to a change in unattended auditory stimuli. Psychophysiology 29(5):523–534

    Article  CAS  PubMed  Google Scholar 

  • Marinkovic K, Halgren E, Maltzman I (2001) Arousal-related P3a to novel auditory stimuli is abolished by a moderately low alcohol dose. Alcohol Alcohol 36(6):529–539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mars RB, Debener S, Gladwin TE, Harrison LM, Haggard P, Rothwell JC, Bestmann S (2008) Trial-by-trial fluctuations in the event-related electroencephalogram reflect dynamic changes in the degree of surprise. J Neurosci 28(47):12539–12545. doi:10.1523/JNEUROSCI.2925-08.2008

    Article  CAS  PubMed  Google Scholar 

  • Miller MW, Rietschel JC, McDonald CG, Hatfield BD (2011) A novel approach to the physiological measurement of mental workload. Int J Psychophysiol 80(1):75–78. doi:10.1016/j.ijpsycho.2011.02.003

    Article  PubMed  Google Scholar 

  • Miltner W, Johnson RJ, Braun C (1991) Auditory and somatosensory event-related potentials: II effects of interstimulus interval. Psychophysiology 5:27–42

    Google Scholar 

  • Muller HJ, Findlay JM (1988) The effect of visual attention on peripheral discrimination thresholds in single and multiple element displays. Acta Psychol (Amst) 69(2):129–155

    Article  CAS  Google Scholar 

  • Muller HJ, Rabbitt PM (1989) Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform 15(2):315–330

    Article  CAS  PubMed  Google Scholar 

  • Muller-Gass A, Schroger E (2007) Perceptual and cognitive task difficulty has differential effects on auditory distraction. Brain Res 1136(1):169–177

    Article  CAS  PubMed  Google Scholar 

  • Naatanen R (1982) Processing negativity: an evoked-potential reflection of selective attention. Psychol Bull 92(3):605–640

    Article  CAS  PubMed  Google Scholar 

  • Näätänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behav Brain Sci 13:201–233

    Article  Google Scholar 

  • Näätänen R (1992) Attention and brain function. Lawrence Erlbaum, Hillsdale

    Google Scholar 

  • Näätänen R, Picton TW (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425

    Article  PubMed  Google Scholar 

  • Näätänen R, Winkler I (1999) The concept of auditory stimulus representation in cognitive neuroscience. Psychol Bull 125(6):826–859

    Article  PubMed  Google Scholar 

  • Nelson DA, Lassman FM (1968) Effects of intersignal interval on the human auditory evoked response. J Acoust Soc Am 44:1529–1532

    Article  CAS  PubMed  Google Scholar 

  • Ofek E, Pratt H (2004) Ear advantage and attention: an ERP study of auditory cued attention. Hear Res 189(1–2):107–118. doi:10.1016/S0378-5955(03)00392-7

    Article  CAS  PubMed  Google Scholar 

  • Parmentier FB, Elford G, Escera C, Andres P, San Miguel I (2008) The cognitive locus of distraction by acoustic novelty in the cross-modal oddball task. Cognition 106(1):408–432

    Article  PubMed  Google Scholar 

  • Parmentier FB, Elsley JV, Ljungberg JK (2010) Behavioral distraction by auditory novelty is not only about novelty: the role of the distracter’s informational value. Cognition 115(3):504–511. doi:10.1016/j.cognition.2010.03.002

    Article  PubMed  Google Scholar 

  • Parmentier FB, Elsley JV, Andres P, Barcelo F (2011) Why are auditory novels distracting? Contrasting the roles of novelty, violation of expectation and stimulus change. Cognition 119(3):374–380. doi:10.1016/j.cognition.2011.02.001

    Article  PubMed  Google Scholar 

  • Parmentier FB, Hebrero M (2013) Cognitive control of involuntary distraction by deviant sounds. J Exp Psychol Learn Mem Cogn 39(5):1635–1641. doi:10.1037/a0032421

    Article  PubMed  Google Scholar 

  • Perrin F, Pernier J, Bertrand O, Echallier JF (1989) Spherical splines for scalp potential and current density map**. Electroencephalogr Clin Neuro 72:184–187

    Article  CAS  Google Scholar 

  • Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118(10):2128–2148. doi:10.1016/j.clinph.2007.04.019

    Article  PubMed Central  PubMed  Google Scholar 

  • Polich J, Aung M, Dalessio DJ (1988) Long latency auditory evoked potentials: intensity, interstimulus interval, and habituation. Pavlov J Biol Sci 23:35–40

    CAS  PubMed  Google Scholar 

  • Ranganath C, Rainer G (2003) Neural mechanisms for detecting and remembering novel events. Nat Rev Neurosci 4(3):193–202. doi:10.1038/nrn1052

    Article  CAS  PubMed  Google Scholar 

  • Restuccia D, Della Marca G, Marra C, Rubino M, Valeriani M (2005) Attentional load of the primary task influences the frontal but not the temporal generators of mismatch negativity. Brain Res Cogn Brain Res 25(3):891–899. doi:10.1016/j.cogbrainres.2005.09.023

    Article  PubMed  Google Scholar 

  • Rinne T, Sarkka A, Degerman A, Schroger E, Alho K (2006) Two separate mechanisms underlie auditory change detection and involuntary control of attention. Brain Res 1077(1):135–143. doi:10.1016/j.brainres.2006.01.043

    Article  CAS  PubMed  Google Scholar 

  • Ruhnau P, Wetzel N, Widmann A, Schroger E (2010) The modulation of auditory novelty processing by working memory load in school age children and adults: a combined behavioral and event-related potential study. BMC Neurosci 11:126. doi:10.1186/1471-2202-11-126

    Article  PubMed Central  PubMed  Google Scholar 

  • SanMiguel I, Corral MJ, Escera C (2008) When loading working memory reduces distraction: behavioral and electrophysiological evidence from an auditory–visual distraction paradigm. J Cogn Neurosci 20(7):1131–1145

    Article  PubMed  Google Scholar 

  • SanMiguel I, Linden D, Escera C (2010a) Attention capture by novel sounds: distraction versus facilitation. Eur J Cogn Psychol 22(4):481–515

    Article  Google Scholar 

  • SanMiguel I, Morgan HM, Klein C, Linden D, Escera C (2010b) On the functional significance of novelty-P3: facilitation by unexpected novel sounds. Biol Psychol 83(2):143–152

    Article  PubMed  Google Scholar 

  • Schröger E (1996) A neural mechanism for involuntary attention shifts to changes in auditory stimulation. J Cogn Neurosci 8(6):527–539. doi:10.1162/jocn.1996.8.6.527

    Article  PubMed  Google Scholar 

  • Schröger E, Bendixen A, Denham SL, Mill RW, Bohm TM, Winkler I (2013) Predictive regularity representations in violation detection and auditory stream segregation: from conceptual to computational models. Brain Topogr. doi:10.1007/s10548-013-0334-6

    PubMed  Google Scholar 

  • Sussman E, Steinschneider M, Gumenyuk V, Grushko J, Lawson K (2008) The maturation of human evoked brain potentials to sounds presented at different stimulus rates. Hear Res 236(1–2):61–79. doi:10.1016/j.heares.2007.12.001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sutton S, Braren M, Zubin J, John ER (1965) Evoked-potential correlates of stimulus uncertainty. Science 150(3700):1187–1188

    Article  CAS  PubMed  Google Scholar 

  • Suwazono S, Machado L, Knight RT (2000) Predictive value of novel stimuli modifies visual event-related potentials and behavior. Clin Neurophysiol 111(1):29–39

    Article  CAS  PubMed  Google Scholar 

  • Wetzel N, Widmann A, Schroger E (2012) Distraction and facilitation: two faces of the same coin? J Exp Psychol Hum Percept Perform 38(3):664–674. doi:10.1037/a0025856

    Article  PubMed  Google Scholar 

  • Wetzel N, Schroger E, Widmann A (2013) The dissociation between the P3a event-related potential and behavioral distraction. Psychophysiology. doi:10.1111/psyp.12072

    PubMed  Google Scholar 

  • Yago E, Escera C, Alho K, Giard MH, Serra-Grabulosa JM (2003) Spatiotemporal dynamics of the auditory novelty-P3 event-related brain potential. Brain Res Cogn Brain Res 16(3):383–390

    Article  PubMed  Google Scholar 

  • Zhang P, Chen X, Yuan P, Zhang D, He S (2006) The effect of visuospatial attentional load on the processing of irrelevant acoustic distractors. Neuroimage 33(2):715–724

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank A. Garnier for his help in recruiting and testing subjects. This work was supported by the European Research Executive Agency grant PCIC10-GA-2011-304201 (FP7-PEOPLE-2011-CIG). This work was performed within the framework of the LABEX CORTEX (ANR-11-LABX-0042) ans the LABEX CELYA (ANR-10-LABX-0060) of Université de Lyon, within the program “Investissements d’Avenir” (ANR-11-IDEX-0007) operated by the French National Research Agency (ANR).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aurélie Bidet-Caulet.

Additional information

This is one of several papers published together in Brain Topography on the ‘‘Special Issue: Auditory Cortex 2012”.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bidet-Caulet, A., Bottemanne, L., Fonteneau, C. et al. Brain Dynamics of Distractibility: Interaction Between Top-Down and Bottom-Up Mechanisms of Auditory Attention. Brain Topogr 28, 423–436 (2015). https://doi.org/10.1007/s10548-014-0354-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-014-0354-x

Keywords

Navigation