Abstract
The present study examined the impact of white noise on word recall performance and brain activity in 40 healthy adolescents, split in two groups (normal and low) depending on their auditory working memory capacity (AWMC). Using functional magnetic resonance imaging, participants performed a backward recall task under four different signal-to-noise ratio (SNR) conditions: 15, 10, 5, and 0-dB SNR. Behaviorally, normal AWMC individuals scored significantly higher than low AWMC individuals across noise levels. Whole-brain analyses showed brain activation not to be statistically different between groups across noise levels. In the normal group, a significant positive relationship was found between performance and number of activated voxels in the right superior frontal gyrus. In the low group, significant positive correlations were found between performance and number of activated voxels in left superior frontal gyrus, left inferior frontal gyrus, and left anterior cingulate cortex. These findings suggest that the strategic structure involved in the enhancement of AWM performance may differ in normal and low AWMC individuals.
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References
Abdul Manan H, Franz EA, Yusoff AN, Mukari SZMS (2012) Hippocampal-cerebellar involvement in enhancement of performance in word-based BRT with the presence of background noise: an initial fMRI study. Psychol Neurosci 5(2):247–256. https://doi.org/10.3922/j.psns.2012.2.16
Abdul Manan H, Franz EA, Yusoff AN, Mukari SZMS (2014) Age-related brain activation during forward and backward verbal memory tasks. Neurol Psychiatry Brain Res 20(4):76–86. https://doi.org/10.1016/j.npbr.2014.08.001
Alagapan S, Lustenberger C, Hadar E, Shin HW, Frӧhlich F (2019) Low-frequency direct cortical stimulation of left superior frontal gyrus enhances working memory performance. Neuroimage 184:697–706. https://doi.org/10.1016/j.neuroimage.2018.09.064
Angwin AJ, Wilson WJ, Arnott WL, Signorini A, Barry RJ, Copland DA (2017) White noise enhances new-word learning in healthy adults. Sci Rep 7(13045):2–7. https://doi.org/10.1038/s41598-017-13383-3
Baijot S, Slama H, Söderlund G, Dan B, Deltenre P, Colin C, Deconinck N (2016) Neuropsychological and neurophysiological benefits from white noise in children with and without ADHD. Behav Brain Funct 12(11):1–13. https://doi.org/10.1186/s12993-016-0095-y
Benzi R, Parisi G, Sutera A, Vulpiani A (1982) Stochastic resonance in climatic change. Tellus 34:10–16. https://doi.org/10.3402/tellusa.v34i1.10782
Boisgueheneuc FD, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129(12):3315–3328. https://doi.org/10.1093/brain/awl244
Brewer AA, Barton B (2016) Maps of the auditory cortex. Annu Rev Neurosci 39:385–407. https://doi.org/10.1146/annurev-neuro-070815-014045
Bryden DW, Johnson EE, Tobia SC, Kashtelyan V, Roesch MR (2011) Attention for learning signals in anterior cingulate cortex. J Neurosci 31(50):18266–18274. https://doi.org/10.1523/JNEUROSCI.4715-11.2011
Buchsbaum BR, Olsen RK, Koch P, Berman FK (2005) Human dorsal and ventral auditory streams subserve rehearsal-based and echoic processes during verbal working memory. Neuron 48(4):687–697. https://doi.org/10.1016/j.neuron.2005.09.029
Donolato E, Giofrè D, Mammarella IC (2017) Differences in verbal and visuospatial forward and backward order recall: a review of the literature. Front Psychol 8:1–14. https://doi.org/10.3389/fpsyg.2017.00663
Douglass JK, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365(6444):337–340. https://doi.org/10.1038/365337a0
Du Y, Zatorre R (2017) Musical training sharpens and bonds ears and tongue to hear speech better. Proc Natl Acad Sci 114(51):13579–13584. https://doi.org/10.1073/pnas.1712223114
Elst WVD, Boxtel MPJV, Breukelen GJPV, Jolles J (2005) Rey’s verbal learning test: Normative data for 1855 healthy participants aged 24–81 years and the influence of age, sex, education, and mode of presentation. J Int Neuropsychol Soc 11(3):290–302. https://doi.org/10.1017/S1355617705050344
Emch M, Bastian CCV, Koch K (2019) Neural correlates of verbal working memory: an fMRI meta-analysis. Front Hum Neurosci 13(180):1–17. https://doi.org/10.3389/fnhum.2019.00180
Faisal A, Selen LPJ, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9(4):292–303. https://doi.org/10.1038/nrn2258.Noise
Fincham JM, Anderson JR (2006) Distinct roles of the anterior cingulate and prefrontal cortex in the acquisition and performance of a cognitive skill. Proc Natl Acad Sci 103(34):12941–12946. https://doi.org/10.1073/pnas.0605493103
Gordon-Salant S, Cole SS (2016) Effects of age and working memory capacity on speech recognition performance in noise among listeners with normal hearing. Ear Hear 37(5):593–602. https://doi.org/10.1097/AUD.0000000000000316
Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW (1999) “Sparse” temporal sampling in auditory fMRI. Hum Brain Mapp 7(3):213–223. https://doi.org/10.1002/(SICI)1097-0193(1999)7:3%3c213:AID-HBM5%3e3.0.CO;2-N
Hallam GP, Thompson HE, Hymers M, Millman RE, Rodd JM, Lambon-Ralph MA, Smallwood J, Jefferies E (2018) Task-based and resting-state fMRI reveal compensatory network changes following damage to left inferior frontal gyrus. Cortex 99:150–165. https://doi.org/10.1016/j.cortex.2017.10.004
Harms MP, Wang L, Csernansky JG, Barch DM (2013) Structure-function relationship of working memory activity with hippocampal and prefrontal cortex volumes. Brain Struct Funct 218(1):173–186. https://doi.org/10.1007/s00429-012-0391-8
Helps SK, Bamford S, Sonuga-Barke EJS, Söderlund GBW (2014) Different effects of adding white noise on cognitive performance of sub-, normal and super-attentive school children. PLoS ONE 9(11):1–10. https://doi.org/10.1371/journal.pone.0112768
Hill AC, Laird AR, Robinson JL (2014) Gender differences in working memory networks: a BrainMap meta-analysis. Biol Psychol 102(334):18–29. https://doi.org/10.1016/j.biopsycho.2014.06.008
Hirshorn EA, Thompson-Schill SL (2006) Role of the left inferior frontal gyrus in covert word retrieval: neural correlates of switching during verbal fluency. Neuropsychologia 44(12):2547–2557. https://doi.org/10.1016/j.neuropsychologia.2006.03.035
Jamaluddin R, Othman Z, Musa KI, Najib M, Alwi M (2009) Validation of the malay version of auditory verbal learning test (MVAVLT) among schizophrenia patients in hospital Universiti Sains Malaysia (HUSM). Malays ASEAN J Psychiatry 10(1):1–21
Joseph S, Teki S, Kumar S, Husain M, Griffiths TD (2016) Resource allocation models of auditory working memory. Brain Res 1640:183–192. https://doi.org/10.1016/j.brainres.2016.01.044
Kumar S, Joseph S, Pearson B, Teki S, Fox ZV, Griffiths TD (2013) Resource allocation and prioritization in auditory working memory. Cogn Neurosci 4(1):12–20. https://doi.org/10.1080/17588928.2012.716416
Kumar S, Joseph S, Gander PE, Barascud N, Halpern AR, Griffiths TD (2016) A brain system for auditory working memory. J Neurosci 36(16):4492–4505. https://doi.org/10.1523/JNEUROSCI.4341-14.2016
Lavin C, Melis C, Mikulan E, Gelormini C, Huepe D, Ibañez A (2013) The anterior cingulate cortex: an integrative hub for human socially-driven interactions. Front Neurosci 7:1–4. https://doi.org/10.3389/fnins.2013.00064
Lenartowicz A, McIntosh AR (2005) The role of anterior cingulate cortex in working memory is shaped by functional connectivity. J Cogn Neurosci 17(7):1026–1042. https://doi.org/10.1162/0898929054475127
Lotfi Y, Mehrkian S, Moossavi A, Zadeh SF, Sadjedi H (2016) Relation between working memory capacity and auditory stream segregation in children with auditory processing disorder. Iran J Med Sci 41(2):110–117
Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239. https://doi.org/10.1016/S1053-8119(03)00169-1
McDonnell MD, Ward LM (2011) The benefits of noise in neural systems: bridging theory and experiment. Nat Rev Neurosci 12(7):415–425. https://doi.org/10.1038/nrn3061
Mitrushina M, Satz P, Chervinsky A, D’Elia L (1991) Performance of four age groups of normal elderly on the Rey Auditory-Verbal learning test. J Clin Psychol 47(3):351–357. https://doi.org/10.1002/1097-4679(199105)47:3%3c351:AID-JCLP2270470305%3e3.0.CO;2-S
Moss F, Ward LM, Sannita WG (2004) Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol 115(2):267–281. https://doi.org/10.1016/j.clinph.2003.09.014
Mostofsky SH, Simmonds DJ (2008) Response inhibition and response selection: two sides of the same coin. J Cogn Neurosci 20(5):751–761. https://doi.org/10.1162/jocn.2008.20500
Pickens TA, Khan SP, Berlau DJ (2019) White noise as a possible therapeutic option for children with ADHD. Complement Ther Med 42:151–155. https://doi.org/10.1016/j.ctim.2018.11.012
Qin S, Basak C (2020) Age-related differences in brain activation during working memory updating: an fMRI study. Neuropsychologia 138:1–12. https://doi.org/10.1016/j.neuropsychologia.2020.107335
Rogers M, Hwang H, Toplak M, Weiss M, Tannock R (2011) Inattention, working memory, and academic achievement in adolescents referred for attention deficit/hyperactivity disorder (ADHD). Child Neuropsychol 17(5):444–458. https://doi.org/10.1080/09297049.2010.544648
Schlittmeier S, Feil A, Liebl A, Hellbrück J (2015) The impact of road traffic noise on cognitive performance in attention-based tasks depends on noise level even within moderate-level ranges. Noise Health 17(76):148–157. https://doi.org/10.4103/1463-1741.155845
Sejdić E, Lipsitz LA (2013) Necessity of noise in physiology and medicine. Comput Methods Progr Biomed 111(2):459–470. https://doi.org/10.1016/j.cmpb.2013.03.014
Sikström S, Söderlund GBW (2007) Stimulus-dependent dopamine release in attention-deficit/hyperactivity disorder. Psychol Rev 114(4):1047–1075. https://doi.org/10.1037/0033-295X.114.4.1047
Söderlund G, Sikström S, Smart A (2007) Listen to the noise: noise is beneficial for cognitive performance in ADHD. J Child Psychol Psychiatry 48(8):840–847. https://doi.org/10.1111/j.1469-7610.2007.01749.x
Söderlund GBW, Sikström S, Loftesnes JM, Sonuga-Barke EJ (2010) The effects of background white noise on memory performance in inattentive school children. Behav Brain Funct 6(55):1–10. https://doi.org/10.1186/1744-9081-6-55
Söderlund GBW, Jobs EN (2016) Differences in speech recognition between children with attention deficits and typically developed children disappear when exposed to 65 db of auditory noise. Front Psychol 7:1–11. https://doi.org/10.3389/fpsyg.2016.00034
Teruya LC, Ortiz KZ, Minett TSC (2009) Performance of normal adults on Rey auditory learning test: a pilot study. Arq Neuropsiquiatr 67(2):224–228. https://doi.org/10.1590/S0004-282X2009000200010
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. https://doi.org/10.1006/nimg.2001.0978
Unsworth N, Engle RW (2007) The nature of individual differences in working memory capacity: active maintenance in primary memory and controlled search from secondary memory. Psychol Rev 114(1):104–132. https://doi.org/10.1037/0033-295X.114.1.104
Vakil E, Blachstein H (1993) Rey auditory-verbal learning test: structure analysis. J Clin Psychol 49(6):883–890. https://doi.org/10.1002/1097-4679(199311)49:6%3c883:AID-JCLP2270490616%3e3.0.CO;2-6
Wegrzyn M, Herbert C, Ethofer T, Flaisch T, Kissler J (2017) Auditory attention enhances processing of positive and negative words in inferior and superior prefrontal cortex. Cortex 96:31–45. https://doi.org/10.1016/j.cortex.2017.08.018
Wylie GR, Genova H, Deluca J, Chiaravalloti N, Sumowski JF (2014) Functional magnetic resonance imaging movers and shakers: does subject-movement cause sampling bias? Hum Brain Mapp 35:1–13. https://doi.org/10.1002/hbm.22150
Yusoff AN, Abd Hamid K, Mohamad M, Abdullah A, Abdul Hamid H, Mukari SZM (2013) Assessing human cortical activation and network during pitch discrimination task in quiet and in noisy background. Mod Appl Sci 7(10):42–59. https://doi.org/10.5539/mas.v7n10p42
Yusoff AN, Hamid KA, Hamzah H, Mohamad M, Mukari SZMS, Abdullah WAKW (2016) Optimization of number of scans for a sparse temporal sampling (STS) functional magnetic resonance imaging (fMRI). Sains Malaysiana 45(10):1525–1530
Acknowledgements
The authors would like to express their gratitude to Dr. Nashrah Maamor, Head of Audiology Program, Faculty of Health Science, Universiti Kebangsaan Malaysia, for providing the hearing test services. We are grateful to Mohamad Nor Affendi Awang and Nooradila Zolkiflee, the radiographers of Universiti Kebangsaan Malaysia Medical Centre for their assistance in MRI scans. We are also thankful to Muhammad Riddha Abdul Rahman for assisting us with the figures formatting.
Funding
This study was funded by the Universiti Kebangsaan Malaysia Incentive Research Grant (GGP-2017-010).
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Othman, E., Yusoff, A.N., Mohamad, M. et al. Effects of white noise on word recall performance and brain activity in healthy adolescents with normal and low auditory working memory. Exp Brain Res 238, 945–956 (2020). https://doi.org/10.1007/s00221-020-05765-3
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DOI: https://doi.org/10.1007/s00221-020-05765-3