Effect of Attention on Prestimulus Neural Noise

Authors

  • Anoop Basavanahalli Jagadeesh Northwestern University
  • Sandeep Maruthy Department of Audiology, All India Institute of Speech and Hearing
  • Ajith Kumar U Department of Audiology, All India Institute of Speech and Hearing

DOI:

https://doi.org/10.15540/nr.11.1.62

Keywords:

auditory evoked potential (AEP), Attention, Neural Noise, Pre-stimulus, Anticipatory, RMS

Abstract

Attending to a target sound increases the number of cortical resources allotted towards processing the target stimuli, leading to larger response amplitudes for the cortical auditory evoked potentials (CAEPs). However, the effect of attention on the neural noise, as well its definition, is still not clear. Having defined neural noise as the neural activity immediately preceding a stimulus, we aimed to explore the effects of attention on the prestimulus activity when measured using CAEPs. Using a 256-channel montage, we compared the global RMS amplitudes of the prestimulus (PreRMS), poststimulus (PostRMS), and the difference between PostRMS and PreRMS (DiffRMS) measured under active attention and passive attention conditions. Paired t-tests revealed a significant attention-related increase in the amplitudes of all three measures. We suppose that the attention-related excitation of target-relevant cortical pathways as well as the inhibition of target-irrelevant mechanisms, in combination, resulted in an increase in the overall neural activity in the three measures. Higher prestimulus activity can, therefore, be used as an objective index of attention and is likely to indicate anticipatory cortical preparation. Our results further validate the supposition that prestimulus activity is not merely neural noise, but indicates the neurophysiological activity associated with complex sensory and/or cognitive functions.

References

Alhanbali, S., Munro, K. J., Dawes, P., Perugia, E., & Millman, R. E. (2022). Associations between pre-stimulus alpha power, hearing level and performance in a digits-in-noise task. International Journal of Audiology, 61(3), 197–204. https://doi.org/10.1080/14992027.2021.1899314

Alho, K. (1992). Selective attention in auditory processing as reflected by event-related brain potentials. Psychophysiology, 29(3), 247–263. https://doi.org/10.1111/j.1469-8986.1992.tb01695.x

American National Standards Institute. (1999). Maximum permissible ambient noise levels for audiometric test rooms (ANSI S3.1-1999).

Bastiaansen, M. C. M., & Brunia, C. H. M. (2001). Anticipatory attention: An event-related desynchronization approach. International Journal of Psychophysiology, 43(1), 91–107. https://doi.org/10.1016/S0167-8760(01)00181-7

Bennet, K. O., Billings, C. J., Molis, M. R., & Leek, M. R. (2012). Neural encoding and perception of speech signals in informational masking. Ear Hear, 32(2), 231–238. https://doi.org/10.1097/AUD.0b013e31823173fd

Debener, S., Herrmann, C. S., Kranczioch, C., Gembris, D., & Engel, A. K. (2003). Top-down attentional processing enhances auditory evoked gamma band activity. NeuroReport, 14(5), 683–686. https://doi.org/10.1097/00001756-200304150-00005

Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009

Dwyer, P., Vukusic, S., Williams, Z. J., Saron, C. D., & Rivera, S. M. (2022). “Neural noise” in auditory responses in young autistic and neurotypical children. Journal of Autism and Developmental Disorders, 54, 642–661 https://doi.org/10.1007/s10803-022-05797-4

Fellinger, R., Klimesch, W., Gruber, W., Freunberger, R., & Doppelmayr, M. (2011). Pre-stimulus alpha phase-alignment predicts P1-amplitude. Brain Research Bulletin, 85(6), 417–423. https://doi.org/10.1016/j.brainresbull.2011.03.025

Ferree, T. C., Luu, P., Russell, G. S., & Tucker, D. M. (2001). Scalp electrode impedance, infection risk, and EEG data quality. Clinical Neurophysiology, 112(3), 536–544. https://doi.org/10.1016/S1388-2457(00)00533-2

Folyi, T., Fehér, B., & Horváth, J. (2012). Stimulus-focused attention speeds up auditory processing. International Journal of Psychophysiology, 84(2), 155–163. https://doi.org/10.1016/j.ijpsycho.2012.02.001

Foxe, J. J., & Snyder, A. C. (2011). The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention. Frontiers in Psychology, 2, 154. https://doi.org/10.3389/fpsyg.2011.00154

Fuglsang, S. A., Dau, T., & Hjortkjær, J. (2017). Noise-robust cortical tracking of attended speech in real-world acoustic scenes. NeuroImage, 156, 435–444. https://doi.org/10.1016/j.neuroimage.2017.04.026

Getzmann, S., Jasny, J., & Falkenstein, M. (2017). Switching of auditory attention in “cocktail-party” listening: ERP evidence of cueing effects in younger and older adults. Brain and Cognition, 111, 1–12. https://doi.org/10.1016/j.bandc.2016.09.006

Haigh, S. M. (2018). Variable sensory perception in autism. European Journal of Neuroscience, 47(6), 602–609. https://doi.org/10.1111/ejn.13601

Harris, A. M., Dux, P. E., & Mattingley, J. B. (2018). Detecting unattended stimuli depends on the phase of prestimulus neural oscillations. The Journal of Neuroscience, 38(12), 3092–3101. https://doi.org/10.1523/JNEUROSCI.3006-17.2018

Harris, K. C., Wilson, S., Eckert, M. A., & Dubno, J. R. (2012). Human evoked cortical activity to silent gaps in noise. Ear & Hearing, 33(3), 330–339. https://doi.org/10.1097/AUD.0b013e31823fb585

Henry, M. J., Herrmann, B., Kunke, D., & Obleser, J. (2017). Aging affects the balance of neural entrainment and top-down neural modulation in the listening brain. Nature Communications, 8, Article 15801. https://doi.org/10.1038/ncomms15801

Hillyard, S. A., Hink, R. F., Schwent, V. L., & Picton, T. W. (1973). Electrical Signs of Selective Attention in the Human Brain. Science, 182(4108), 177–180. https://doi.org/10.1126/science.182.4108.177

Horton, C., D’Zmura, M., & Srinivasan, R. (2013). Suppression of competing speech through entrainment of cortical oscillations. Journal of Neurophysiology, 109(12), 3082–3093. https://doi.org/10.1152/jn.01026.2012

Kayser, S. J., McNair, S. W., & Kayser, C. (2016). Prestimulus influences on auditory perception from sensory representations and decision processes. Proceedings of the National Academy of Sciences, 113(17), 4842–4847. https://doi.org/10.1073/pnas.1524087113

Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53(1), 63–88. https://doi.org/10.1016/j.brainresrev.2006.06.003

Krizman, J., Bonacina, S., Otto-Meyer, R., & Kraus, N. (2021). Non-stimulus-evoked activity as a measure of neural noise in the frequency-following response. Journal of Neuroscience Methods, 362, 109290. https://doi.org/10.1016/j.jneumeth.2021.109290

Krizman, J., Lindley, T., Bonacina, S., Colegrove, D., White-Schwoch, T., & Kraus, N. (2020). Play sports for a quieter brain: Evidence from Division I collegiate athletes. Sports Health, 12(2), 154–158. https://doi.org/10.1177/1941738119892275

Lehmann, D., & Skrandies, W. (1980). Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalography and Clinical Neurophysiology, 48(6), 609–621. https://doi.org/10.1016/0013-4694(80)90419-8

Luck, S. J., Chelazzi, L., Hillyard, S. A., & Desimone, R. (1997). Neural mechanisms of spatial selective attention in areas v1, v2, and v4 of macaque visual cortex. Journal of Neurophysiology, 77(1), 24–42. https://doi.org/10.1152/jn.1997.77.1.24

Mast, T., & Watson, C. (1968). Attention and auditory evoked responses to low-detectability signals. Perception & Psychophysics, 4(4), 237–240. https://doi.org/10.3758/BF03206309

Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M., & Ro, T. (2009). To see or not to see: Prestimulus alpha phase predicts visual awareness. The Journal of Neuroscience, 29(9), 2725–2732. https://doi.org/10.1523/jneurosci.3963-08.2009

McNair, S. W., Kayser, S. J., & Kayser, C. (2019). Consistent pre-stimulus influences on auditory perception across the lifespan. NeuroImage, 186, 22–32. https://doi.org/10.1016/j.neuroimage.2018.10.085

Musacchia, G., Sams, M., Nicol, T., & Kraus, N. (2006). Seeing speech affects acoustic information processing in the human brainstem. Experimental Brain Research, 168(1–2), 1–10. https://doi.org/10.1007/s00221-005-0071-5

Nandy, A., Nassi, J. J., Jadi, M. P., & Reynolds, J. (2019). Optogenetically induced low-frequency correlations impair perception. ELife, 8, Article e35123. https://doi.org/10.7554/eLife.35123

Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113. https://doi.org/10.1016/0028-3932(71)90067-4

Olguin, A., Bekinschtein, T. A., & Bozic, M. (2018). Neural encoding of attended continuous speech under different types of interference. Journal of Cognitive Neuroscience, 30(11), 1606–1619. https://doi.org/10.1162/jocn_a_01303

Pfurtscheller, G., & Da Silva, F. L. (2011). EEG-event-related desynchronization (ERD) and event-related synchronization. In D. L. Schomer, & F. L. Da Silva (Eds.), Niedermeyer’s Electroencephalography - Basic principles, clinical applications and related fields (6th ed., pp. 935–948). Kluwer/Lippincott Williams & Wilkins.

Pfurtscheller, G., Stancák, A., & Neuper, Ch. (1996). Event-related synchronization (ERS) in the alpha band — an electrophysiological correlate of cortical idling: A review. International Journal of Psychophysiology, 24(1–2), 39–46. https://doi.org/10.1016/S0167-8760(96)00066-9

Rahn, E., & Başar, E. (1993). Prestimulus EEG-activity strongly influences the auditory evoked vertex response: A new method for selective averaging. The International Journal of Neuroscience, 69(1–4), 207–220. https://doi.org/10.3109/00207459309003331

Russo, N., Nicol, T., Musacchia, G., & Kraus, N. (2004). Brainstem responses to speech syllables. Clinical Neurophysiology, 115(9), 2021–2030. https://doi.org/10.1016/j.clinph.2004.04.003

Skoe, E., Krizman, J., & Kraus, N. (2013). The impoverished brain: Disparities in maternal education affect the neural response to sound. Journal of Neuroscience, 33(44), 17221–17231. https://doi.org/10.1523/JNEUROSCI.2102-13.2013

Sussman, E. S., Bregman, A. S., Wang, W. J., & Khan, F. J. (2005). Attentional modulation of electrophysiological activity in auditory cortex for unattended sounds within multistream auditory environments. Cognitive, Affective & Behavioral Neuroscience, 5(1), 93–110. https://doi.org/10.3758/CABN.5.1.93

The JASP Team. (2017). JASP (Version 0.8.5.1). [Computer Software].

Vaidyanath, R., & Yathiraj, A. (2014). Screening checklist for auditory processing in adults (SCAP-A): Development and preliminary findings. Journal of Hearing Science, 4(1), 27–37. https://doi.org/10.17430/890788

Zendel, B. R., de Boysson, C., Mellah, S., Démonet, J. F., & Belleville, S. (2016). The impact of attentional training on event-related potentials in older adults. Neurobiology of Aging, 47, 10–22. https://doi.org/10.1016/j.neurobiolaging.2016.06.023

Zhang, C., Arnott, S. R., Rabaglia, C., Avivi-Reich, M., Qi, J., Wu, X., Li, L., & Schneider, B. A. (2016). Attentional modulation of informational masking on early cortical representations of speech signals. Hearing Research, 331, 119–130. https://doi.org/10.1016/j.heares.2015.11.002

Zhao, Y., Song, Q., Li, X., & Li, C. (2016). Neural hyperactivity of the central auditory system in response to peripheral damage. Neural Plasticity, 2016, Article 2162105. https://doi.org/10.1155/2016/2162105

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Published

2024-03-29

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Research Papers