Abstract
Introduction
Although the effects of scanner background noise (SBN) during functional magnetic resonance imaging (fMRI) have been extensively investigated for the brain regions involved in auditory processing, its impact on other types of intrinsic brain activity has largely been neglected. The present study evaluated the influence of SBN on a number of intrinsic connectivity networks (ICNs) during auditory stimulation by comparing the results obtained using sparse temporal acquisition (STA) with those using continuous acquisition (CA).
Methods
Fourteen healthy subjects were presented with classical music pieces in a block paradigm during two sessions of STA and CA. A volume-matched CA dataset (CAm) was generated by subsampling the CA dataset to temporally match it with the STA data. Independent component analysis was performed on the concatenated STA–CAm datasets, and voxel data, time courses, power spectra, and functional connectivity were compared.
Results
The ICA revealed 19 ICNs; the auditory, default mode, salience, and frontoparietal networks showed greater activity in the STA. The spectral peaks in 17 networks corresponded to the stimulation cycles in the STA, while only five networks displayed this correspondence in the CA. The dorsal default mode and salience networks exhibited stronger correlations with the stimulus waveform in the STA.
Conclusions
SBN appeared to influence not only the areas of auditory response but also the majority of other ICNs, including attention and sensory networks. Therefore, SBN should be regarded as a serious nuisance factor during fMRI studies investigating intrinsic brain activity under external stimulation or task loads.
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References
Gaab N, Gabrieli JD, Glover GH (2007) Assessing the influence of scanner background noise on auditory processing. II. An fMRI study comparing auditory processing in the absence and presence of recorded scanner noise using a sparse design. Hum Brain Mapp 28:721–732
Talavage TM, Edmister WB, Ledden PJ, Weisskoff RM (1999) Quantitative assessment of auditory cortex responses induced by imager acoustic noise. Hum Brain Mapp 7:79–88
Bandettini PA, Jesmanowicz A, Van Kylen J, Birn RM, Hyde JS (1998) Functional MRI of brain activation induced by scanner acoustic noise. Magn Reson Med 39:410–416
Baumgart F, Gaschler B, Tempelmann C, Tegeler C, Stiller D, Heinze H, Scheich H (1996) Masking of acoustic stimuli by the gradient noise alters the fMRI detectable activation in a particular human auditory cortex. MAGMA 4:185
Tamer G, Talavage TM, Ulmer JL (2004) Characterizing the attenuation and/or saturation effect of the acoustic scanner noise in auditory event-related functional magnetic resonance imaging. Conf Proc IEEE Eng Med Biol Soc 3:1868–1871
Langers DR, Van Dijk P, Backes WH (2005) Interactions between hemodynamic responses to scanner acoustic noise and auditory stimuli in functional magnetic resonance imaging. Magn Reson Med 53:49–60
Shah NJ, Jancke L, Grosse-Ruyken ML, Muller-Gartner HW (1999) Influence of acoustic masking noise in fMRI of the auditory cortex during phonetic discrimination. J Magn Reson Imaging 9:19–25
Cho ZH, Chung SC, Lim DW, Wong EK (1998) Effects of the acoustic noise of the gradient systems on fMRI: a study on auditory, motor, and visual cortices. Magn Reson Med 39:331–335
Zhang N, Zhu XH, Chen W (2005) Influence of gradient acoustic noise on fMRI response in the human visual cortex. Magn Reson Med 54:258–263
Mazard A, Mazoyer B, Etard O, Tzourio-Mazoyer N, Kosslyn SM, Mellet E (2002) Impact of fMRI acoustic noise on the functional anatomy of visual mental imagery. J Cogn Neurosci 14:172–186
Fuchino Y, Sato H, Maki A, Yamamoto Y, Katura T, Obata A, Koizumi H, Yoro T (2006) Effect of fMRI acoustic noise on sensorimotor activation examined using optical topography. Neuroimage 32:771–777
Novitski N, Anourova I, Martinkauppi S, Aronen HJ, Naatanen R, Carlson S (2003) Effects of noise from functional magnetic resonance imaging on auditory event-related potentials in working memory task. Neuroimage 20:1320–1328
Tomasi D, Caparelli EC, Chang L, Ernst T (2005) fMRI-acoustic noise alters brain activation during working memory tasks. Neuroimage 27:377–386
Skouras S, Gray M, Critchley H, Koelsch S (2013) FMRI scanner noise interaction with affective neural processes. PLoS ONE 8:e80564
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 7:213–223
Gaab N, Gabrieli JD, Glover GH (2007) Assessing the influence of scanner background noise on auditory processing. I. An fMRI study comparing three experimental designs with varying degrees of scanner noise. Hum Brain Mapp 28:703–720
Zaehle T, Schmidt CF, Meyer M, Baumann S, Baltes C, Boesiger P, Jancke L (2007) Comparison of “silent” clustered and sparse temporal fMRI acquisitions in tonal and speech perception tasks. Neuroimage 37:1195–1204
Blackman GA, Hall DA (2011) Reducing the effects of background noise during auditory functional magnetic resonance imaging of speech processing: qualitative and quantitative comparisons between two image acquisition schemes and noise cancellation. J Speech Lang Hear Res 54:693–704
Fransson P (2005) Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 26:15–29
Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103:13848–13853
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541
Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. AJNR Am J Neuroradiol 22:1326–1333
Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045
Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, Glahn DC, Beckmann CF, Smith SM, Fox PT (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022–4037
Langers DR, van Dijk P (2011) Robustness of intrinsic connectivity networks in the human brain to the presence of acoustic scanner noise. Neuroimage 55:1617–1632
Yakunina N, Tae WS, Lee KU, Kim SS, Nam EC (2013) Spatiotemporal segregation of neural response to auditory stimulation: an fMRI study using independent component analysis and frequency-domain analysis. PLoS ONE 8:e66424
Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R, Michael AM, Caprihan A, Turner JA, Eichele T, Adelsheim S, Bryan AD, Bustillo J, Clark VP, Feldstein Ewing SW, Filbey F, Ford CC, Hutchison K, Jung RE, Kiehl KA, Kodituwakku P, Komesu YM, Mayer AR, Pearlson GD, Phillips JP, Sadek JR, Stevens M, Teuscher U, Thoma RJ, Calhoun VD (2011) A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2
Zuo XN, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP (2010) Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 49:2163–2177
Guo CC, Kurth F, Zhou J, Mayer EA, Eickhoff SB, Kramer JH, Seeley WW (2012) One-year test-retest reliability of intrinsic connectivity network fMRI in older adults. Neuroimage 61:1471–1483
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673–9678
Fukunaga M, Horovitz SG, van Gelderen P, de Zwart JA, Jansma JM, Ikonomidou VN, Chu R, Deckers RH, Leopold DA, Duyn JH (2006) Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. Magn Reson Imaging 24:979–992
Goldstein B, Shulman A (1996) Tinnitus-hyperacusis and the loudness discomfort level test—a preliminary report. Int Tinnitus J 2:83–89
Calhoun VD (2004) Group ICA of fMRI toolbox (GIFT)
Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14:140–151
Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129–1159
Himberg J, Hyvarinen A (2003) Icasso: software for investigating the reliability of ICA estimates by clustering and visualization. Neural Networks for Signal Processing, 2003 NNSP’03 2003 I.E. 13th Workshop on:259-268
Jafri MJ, Pearlson GD, Stevens M, Calhoun VD (2008) A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39:1666–1681
Henkelman RM (1985) Measurement of signal intensities in the presence of noise in MR images. Med Phys 12:232–233
Reeder SB (2007) Measurement of signal-to-noise ratio and parallel imaging. In: Parallel Imaging in Clinical MR Applications. Springer, pp 49-61
De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:1359–1367
Parsons LM (2001) Exploring the functional neuroanatomy of music performance, perception, and comprehension. Ann N Y Acad Sci 930:211–231
Petacchi A, Laird AR, Fox PT, Bower JM (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 25:118–128
Sens PM, Almeida CI, Souza MM, Goncalves JB, Carmo LC (2011) The role of the cerebellum in auditory processing using the SSI test. Braz J Otorhinolaryngol 77:584–588
KH E, Chen SH, Ho MH, Desmond JE (2014) A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 35:593–615
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676–682
Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38
Uddin LQ, Kelly AM, Biswal BB, Xavier Castellanos F, Milham MP (2009) Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Hum Brain Mapp 30:625–637
Laird AR, Eickhoff SB, Li K, Robin DA, Glahn DC, Fox PT (2009) Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J Neurosci 29:14496–14505
Leech R, Kamourieh S, Beckmann CF, Sharp DJ (2011) Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 31:3217–3224
Leech R, Sharp DJ (2014) The role of the posterior cingulate cortex in cognition and disease. Brain 137:12–32
Gaab N, Gabrieli JD, Glover GH (2008) Resting in peace or noise: scanner background noise suppresses default-mode network. Hum Brain Mapp 29:858–867
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356
Eckert MA, Menon V, Walczak A, Ahlstrom J, Denslow S, Horwitz A, Dubno JR (2009) At the heart of the ventral attention system: the right anterior insula. Hum Brain Mapp 30:2530–2541
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667
Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 105:12569–12574
Bonnelle V, Leech R, Kinnunen KM, Ham TE, Beckmann CF, De Boissezon X, Greenwood RJ, Sharp DJ (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31:13442–13451
Jilka SR, Scott G, Ham T, Pickering A, Bonnelle V, Braga RM, Leech R, Sharp DJ (2014) Damage to the Salience Network and interactions with the Default Mode Network. J Neurosci 34:10798–10807
Spreng RN, Sepulcre J, Turner GR, Stevens WD, Schacter DL (2013) Intrinsic architecture underlying the relations among the default, dorsal attention, and frontoparietal control networks of the human brain. J Cogn Neurosci 25:74–86
Cole MW, Repovs G, Anticevic A (2014) The frontoparietal control system: a central role in mental health. Neuroscientist 20:652–664
Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL (2008) Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol 100:3328–3342
Zhang S, Li CS (2012) Functional networks for cognitive control in a stop signal task: independent component analysis. Hum Brain Mapp 33:89–104
Kim DI, Manoach DS, Mathalon DH, Turner JA, Mannell M, Brown GG, Ford JM, Gollub RL, White T, Wible C, Belger A, Bockholt HJ, Clark VP, Lauriello J, O’Leary D, Mueller BA, Lim KO, Andreasen N, Potkin SG, Calhoun VD (2009) Dysregulation of working memory and default-mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study. Hum Brain Mapp 30:3795–3811
Xu J, Calhoun VD, Pearlson GD, Potenza MN (2014) Opposite modulation of brain functional networks implicated at low vs. high demand of attention and working memory. PLoS ONE 9:e87078
Fassbender C, Simoes-Franklin C, Murphy K, Hester R, Meaney J, Robertson I, Garavan H (2006) The role of a right fronto-parietal network in cognitive control. J Psychophysiol 20:286–296
Diekhof EK, Biedermann F, Ruebsamen R, Gruber O (2009) Top-down and bottom-up modulation of brain structures involved in auditory discrimination. Brain Res 1297:118–123
Brunetti M, Della Penna S, Ferretti A, Del Gratta C, Cianflone F, Belardinelli P, Caulo M, Pizzella V, Olivetti Belardinelli M, Romani GL (2008) A frontoparietal network for spatial attention reorienting in the auditory domain: a human fMRI/MEG study of functional and temporal dynamics. Cereb Cortex 18:1139–1147
Mangano GR, Oliveri M, Turriziani P, Smirni D, Zhaoping L, Cipolotti L (2014) Impairments in top down attentional processes in right parietal patients: paradoxical functional facilitation in visual search. Vis Res 97:74–82
Iidaka T, Matsumoto A, Nogawa J, Yamamoto Y, Sadato N (2006) Frontoparietal network involved in successful retrieval from episodic memory. Spatial and temporal analyses using fMRI and ERP. Cereb Cortex 16:1349–1360
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215
Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324
Vossel S, Geng JJ, Fink GR (2014) Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist 20:150–159
Shulman GL, Ollinger JM, Akbudak E, Conturo TE, Snyder AZ, Petersen SE, Corbetta M (1999) Areas involved in encoding and applying directional expectations to moving objects. J Neurosci 19:9480–9496
Connolly JD, Goodale MA, Menon RS, Munoz DP (2002) Human fMRI evidence for the neural correlates of preparatory set. Nat Neurosci 5:1345–1352
Eckert MA, Kamdar NV, Chang CE, Beckmann CF, Greicius MD, Menon V (2008) A cross‐modal system linking primary auditory and visual cortices: evidence from intrinsic fMRI connectivity analysis. Hum Brain Mapp 29:848–857
Beer AL, Plank T, Meyer G, Greenlee MW (2013) Combined diffusion-weighted and functional magnetic resonance imaging reveals a temporal-occipital network involved in auditory-visual object processing. Frontiers in integrative neuroscience 7
Beer AL, Plank T, Greenlee MW (2011) Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex. Exp Brain Res 213:299–308
Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9:255–266
Koelewijn T, Bronkhorst A, Theeuwes J (2010) Attention and the multiple stages of multisensory integration: a review of audiovisual studies. Acta Psychol 134:372–384
Spence C, Driver J (1997) Audiovisual links in exogenous covert spatial orienting. Percept Psychophys 59:1–22
Driver J, Spence C (1998) Cross-modal links in spatial attention. Philos Trans R Soc Lond B Biol Sci 353:1319–1331
McDonald JJ, Green JJ, Stormer VS, Hillyard SA (2012) Cross-modal spatial cueing of attention influences visual perception. In: Murray MM, Wallace MT (eds) The neural bases of multisensory processes. Taylor & Francis Group, LLC, Boca Raton
Feng W, Stormer VS, Martinez A, McDonald JJ, Hillyard SA (2014) Sounds activate visual cortex and improve visual discrimination. J Neurosci 34:9817–9824
Foxe JJ, Morocz IA, Murray MM, Higgins BA, Javitt DC, Schroeder CE (2000) Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res Cogn Brain Res 10:77–83
Foxe JJ, Wylie GR, Martinez A, Schroeder CE, Javitt DC, Guilfoyle D, Ritter W, Murray MM (2002) Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J Neurophysiol 88:540–543
Spence C, Nicholls ME, Gillespie N, Driver J (1998) Cross-modal links in exogenous covert spatial orienting between touch, audition, and vision. Percept Psychophys 60:544–557
Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278–285
Woodruff PWR (1994) Structural magnetic resonance imaging in psychiatry—the functional psychoses. In: Dawbarn D, Kerwin R (eds) Cambridge medical reviews: neurobiology and psychiatry. Cambridge University Press
Chen L, Bernstein M, Huston J, Fain S (2001) Measurements of T1 relaxation times at 3.0 T: implications for clinical MRA
Acknowledgments
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (2014R1A1A4A01003909).
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We declare that all human and animal studies have been approved by the Kangwon National University Hospital Institutional Review Board and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.
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Yakunina, N., Kang, E.K., Kim, T.S. et al. Effects of scanner acoustic noise on intrinsic brain activity during auditory stimulation. Neuroradiology 57, 1063–1073 (2015). https://doi.org/10.1007/s00234-015-1561-1
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DOI: https://doi.org/10.1007/s00234-015-1561-1