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.
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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
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
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
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
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
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
Brunia CH, van Boxtel GJ (2001) Wait and see. Int J Psychophysiol 43(1):59–75
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
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
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
Coull JT (1998) Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology. Prog Neurobiol 55(4):343–361
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
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
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
Duncan-Johnson CC, Donchin E (1977) On quantifying surprise: the variation of event-related potentials with subjective probability. Psychophysiology 14(5):456–467
Edgington ES (1995) Randomization tests: revised and expanded. Statistics: textbooks and monographs, vol 147, 3rd edn. Marcel Dekker, New York
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
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
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
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
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
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
Giard MH, Fort A, Mouchetant-Rostaing Y, Pernier J (2000) Neurophysiological mechanisms of auditory selective attention in humans. Front Biosci 5:D84–94
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
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
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
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
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
Hillyard SA, Hink RF, Schwent VL, Picton TW (1973) Electrical signs of selective attention in the human brain. Science 182(108):177–180
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
Horvath J (2013) Sensory ERP effects in auditory distraction: did we miss the main event? Psychol Res. doi:10.1007/s00426-013-0507-7
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
Hugdahl K, Nordby H (1994) Electrophysiological correlates to cued attentional shifts in the visual and auditory modalities. Behav Neural Biol 62(1):21–32
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
Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186. doi:10.3389/fnhum.2010.00186
Knight R (1996) Contribution of human hippocampal region to novelty detection. Nature 383(6597):256–259. doi:10.1038/383256a0
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
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
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
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
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
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
Miltner W, Johnson RJ, Braun C (1991) Auditory and somatosensory event-related potentials: II effects of interstimulus interval. Psychophysiology 5:27–42
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
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
Muller-Gass A, Schroger E (2007) Perceptual and cognitive task difficulty has differential effects on auditory distraction. Brain Res 1136(1):169–177
Naatanen R (1982) Processing negativity: an evoked-potential reflection of selective attention. Psychol Bull 92(3):605–640
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
Näätänen R (1992) Attention and brain function. Lawrence Erlbaum, Hillsdale
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
Näätänen R, Winkler I (1999) The concept of auditory stimulus representation in cognitive neuroscience. Psychol Bull 125(6):826–859
Nelson DA, Lassman FM (1968) Effects of intersignal interval on the human auditory evoked response. J Acoust Soc Am 44:1529–1532
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
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
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
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
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
Perrin F, Pernier J, Bertrand O, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neuro 72:184–187
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
Polich J, Aung M, Dalessio DJ (1988) Long latency auditory evoked potentials: intensity, interstimulus interval, and habituation. Pavlov J Biol Sci 23:35–40
Ranganath C, Rainer G (2003) Neural mechanisms for detecting and remembering novel events. Nat Rev Neurosci 4(3):193–202. doi:10.1038/nrn1052
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
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
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
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
SanMiguel I, Linden D, Escera C (2010a) Attention capture by novel sounds: distraction versus facilitation. Eur J Cogn Psychol 22(4):481–515
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
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
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
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
Sutton S, Braren M, Zubin J, John ER (1965) Evoked-potential correlates of stimulus uncertainty. Science 150(3700):1187–1188
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
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
Wetzel N, Schroger E, Widmann A (2013) The dissociation between the P3a event-related potential and behavioral distraction. Psychophysiology. doi:10.1111/psyp.12072
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
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
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).
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This is one of several papers published together in Brain Topography on the ‘‘Special Issue: Auditory Cortex 2012”.
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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
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DOI: https://doi.org/10.1007/s10548-014-0354-x