[en] Tinnitus, the perception of sound in the absence of external stimuli, is often a disturbing symptom for which the underlying functional neuroanatomy still remains poorly understood. Most studies have focused solely on functional connectivity changes in the auditory cortex of tinnitus patients. The aim of this study was to investigate whether a correlation exists between tinnitus behavioural scores and functional brain connectivity of five resting-state networks comprising the auditory, the default mode, the external control left and right, and the salience network. For this purpose, a large sample of one hundred and thirty-five subjects underwent resting-state functional magnetic resonance imaging and their behavioural scores were obtained using clinical evaluations. Networks were extracted using independent component analysis, and functional connectivity patterns in the extracted networks were evaluated by a graph theoretical approach. The effects of tinnitus for each network were investigated by correlating the graph strength of all the regions with the tinnitus behavioural scores using stepwise fit regression analysis. Results indicated that alterations of functional interactions between key neural circuits of the brain are not limited to one single network. In particular, tinnitus distress showed a strong correlation with the connectivity pattern within and between the right executive control network and the other four resting-state networks, indicating that tinnitus distress is probably the consequence of a hyperactive attention condition. Among the behavioural scores, the strongest correlation was observed between age and hearing loss, while the tinnitus objective loudness was not correlated with any behavioural scores.
Research Center/Unit :
GIGA Consciousness, Sensation and Perception Research Group
Disciplines :
Otolaryngology
Author, co-author :
MAUDOUX, Audrey ; Centre Hospitalier Universitaire de Liège - CHU > Autres Services Médicaux > Service d'ORL, d'audiophonologie et de chir. cervico-faciale
KANDEEPAN, Sivayini; University of Western Ontario > Physics and Astronomy > Brain and Mind Institute
Ribeiro de Paula, Demetrius
ZHENG, J.Y.
CABAY, Jean-Evrard ; Centre Hospitalier Universitaire de Liège - CHU > Département de Physique Médicale > Service médical de médecine nucléaire et imagerie onco
GOMEZ, F.
CHRONIK, B.A.
DE RIDDER, D.
VANNESTE, S.
Soddu, Andrea
Language :
English
Title :
Tinnitus distress : a paradoxical attention to the sound?
F.R.S.-FNRS - Fonds de la Recherche Scientifique FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen Tinnitus Research Initiative UA - University of Antwerp EC - European Commission NSERC - Natural Sciences and Engineering Research Council
Funding text :
This research was funded by Research Foundation
Flanders (FWO), Tinnitus Research Initiative (TRI), TOP financiering
from University Antwerp, the Belgian National Funds for Scientific
Research—FNRS (F 5/4/150/5—MCF/SD—9853), the Tinnitus Prize
2011 (FNRS 9.4501.12), and the European Commission. Finally, we
gratefully acknowledge the financial support provided by NSERC Discovery
grant (05578-2014RGPIN).
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Bibliography
Jastreboff, P.J., Phantom auditory perception (tinnitus): mechanisms of generation and perception (1990) Neurosci Res, 8 (4), pp. 221-254
Shargorodsky, J., Curhan, G.C., Farwell, W.R., Prevalence and characteristics of tinnitus among US adults (2010) Am J Med, 123 (8), pp. 711-718
Langguth, B., Kreuzer, P.M., Kleinjung, T., De Ridder, D., Tinnitus: causes and clinical management (2013) Lancet Neurol, 12 (9), pp. 920-930
De Ridder, D., Elgoyhen, A.B., Romo, R., Langguth, B., Phantom percepts: tinnitus and pain as persisting aversive memory networks (2011) Proc Natl Acad Sci USA, 108 (20), pp. 8075-8080
Eggermont, J.J., Roberts, L.E., The neuroscience of tinnitus (2004) Trends Neurosci, 27 (11), pp. 676-682
Mirz, F., Pedersen, C.B., Ishizu, K., Johannsen, P., Ovesen, T., StÖdkilde-JÖrgensen, H., Gjedde, A., Positron emission tomography of cortical centers of tinnitus (1999) Heart Res, 134 (1-2), pp. 133-144
Schlee, W., Lorenz, I., Hartmann, T., Müller, N., Schulz, H., Weisz, N., A global brain model of Tinnitus (2010) Textbook of tinnitus, , Møller AR, Langguth B, Ridder D, Kleinjung T, (eds), Springer, New York, NY
Vanneste, S., De Ridder, D., The auditory and non-auditory brain areas involved in tinnitus. An emergent property of multiple parallel overlapping subnetworks (2012) Front Syst Neurosci, 6, p. 31
Adjamian, P., Sereda, M., Hall, D.A., The mechanisms of tinnitus: perspectives from human functional neuroimaging (2009) Heart Res, 253 (1-2), pp. 15-31
Schlee, W., Weisz, N., Bertrand, O., Hartmann, T., Elbert, T., Using auditory steady state responses to outline the functional connectivity in the tinnitus brain (2008) PLoS One, 3 (11)
Schlee, W., Mapping cortical hubs in tinnitus (2009) BMC Biol, 7, p. 80
Langguth, B., Neuroimaging and neuromodulation: complementary approaches for identifying the neuronal correlates of tinnitus (2012) Front Syst Neurosci, 6, p. 15
Elgoyhen, A.B., Langguth, B., De Ridder, D., Vanneste, S., Tinnitus: perspectives from human neuroimaging (2015) Nat Rev Neurosci, 16 (10), pp. 632-642
Buckner, R.L., Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease (2009) J Neurosci, 29 (6), pp. 1860-1873
Bressler, S.L., Menon, V., Large-scale brain networks in cognition: emerging methods and principles (2010) Trends Cogn Sci, 14, pp. 277-290
Fox, M.D., Raichle, M.E., Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging (2007) Nat Rev Neurosci, 8, pp. 700-711
Biswal, B., Yetkin, F.Z., Haughton, V.M., Hyde, J.S., Functional connectivity in the motor cortex of resting human brain using echo-planar MRI (1995) Magn Reson Med, 34, pp. 537-541
Damoiseaux, J.S., Rombouts, S.A., Barkhof, F., Consistent resting-state networks across healthy subjects (2006) Proc Natl Acad Sci USA, 103 (37), pp. 13848-13853
Moussa, M.N., Steen, M.R., Laurienti, P.J., Hayasaka, S., Consistency of network modules in resting-state FMRI connectome data (2012) PLoS One, 7 (8)
Vanneste, S., Plazier, M., van der Loo, E., Van de Heyning, P., De Ridder, D., The difference between uni- and bilateral auditory phantom percept (2011) Clin Neurophysiol, 122 (3), pp. 578-587
Vanneste, S., van de Heyning, P., De Ridder, D., The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients (2011) Eur J Neurosci, 34 (5), pp. 718-731
Schecklmann, M., Neural correlates of tinnitus duration and distress: a positron emission tomography study (2013) Hum Brain Mapp, 34 (1), pp. 233-240
Maudoux, A., Lefebvre, P., Demertzi, A., Cabay, J.E., Vanhaudenhuyse, A., Laureys, S., Soddu, A., Connectivity graph analysis of the auditory resting state network in tinnitus (2012) Brain Res, 1485, pp. 10-21
Schmidt, S.A., Akrofi, K., Carpenter-Thompson, J.R., Husain, F.T., Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss (2013) PLoS One, 8 (10)
Hallam, R.S., (1996) Manual of the Tinnitus Questionnaire (TQ), , Psychological Corporation, London
Ribeiro de Paula, D., Ziegler, E., Abeyasinghe, P.M., A method for independent component graph analysis of resting-state fMRI (2017) Brain Behav, 7 (3)
Beckmann, C.F., DeLuca, M., Devlin, J.T., Smith, S.M., Investigations into resting-state connectivity using independent component analysis (2005) Philos Trans R Soc Lond B Biol Sci, 360 (1457), pp. 1001-1013
Holmes, A., Friston, K., Generalisability, random effects and population inference (1998) NeuroImage, 7, p. 754
Demertzi, A., Gomez, F., Crone, J.S., Vanhaudenhuyse, A., Tshibanda, L., Noirhomme, Q., Thonnard, M., Soddu, A., Multiple fMRI system-level baseline connectivity is disrupted in patients with consciousness alterations (2014) Cortex, 52, pp. 35-46
Soddu, A., Vanhaudenhuyse, A., Bahri, M., Bruno, M.A., Boly, M., Demertzi, A., Tshibanda, J.F., Identifying the default mode component in spatial IC analysis of patients with disorders of consciousness (2012) Hum Brain Mapp, 33 (4), pp. 778-796
Maudoux, A., Auditory resting-state network connectivity in tinnitus: a functional MRI study (2012) PLoS One, 7 (5)
Gerhard, S., Daducci, A., Lemkaddem, A., Meuli, R., Thiran, J.P., Hagmann, P., The connectome viewer toolkit: an open source framework to manage, analyze, and visualize connectomes (2011) Front Neuroinform, 5, p. 3
Cavaliere, C., Kandeepan, S., Multimodal neuroimaging approach to variability of functional connectivity in disorders of consciousness: a PET/MRI Pilot study (2018) Front Neurol, 9, p. 861
Chen, Y.-C., Chen, H., Bo, F., Tinnitus distress is associated with enhanced resting-state functional connectivity within the default mode network (2018) Neuropsychiatr Dis Treat, 14, pp. 1919-1927
Trevis, K.J., McLachlan, N.M., Wilson, S.J., Cognitive mechanisms in chronic tinnitus: psychological markers of a failure to switch attention (2016) Front Psychol, 7, p. 1262
Hair, J.F., Jr., Anderson, R.E., Tatham, R.L., Black, W.C., (1995) Multivariate Data Analysis, , 3, Macmillan, New York
Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing (1995) J R Stat Soc Ser B, 57, pp. 289-300
Grades of hearing impairment (1991) Hearing Network News, 1
Bhatt, J.M., Lin, H.W., Bhattacharyya, N., Tinnitus epidemiology: Prevalence, severity, exposures and treatment patterns in the United States: Bhatt JM: Tinnitus in the United States (2016) JAMA Otolaryngol Head Neck Surg, 142 (10), pp. 959-965. , https://doi.org/10.1001/jamaoto.2016.1700
Zanto, T.P., Gazzaley, A., Fronto-parietal network: flexible hub of cognitive control (2013) Trends Cogn Sci, 17 (12), pp. 602-603
Boveroux, P., Vanhaudenhuyse, A., Bruno, M.A., Noirhomme, Q., Lauwick, S., Luxen, A., Degueldre, C., Boly, M., Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness (2010) Anesthesiology, 113, pp. 1038-1053
Liu, X., Lauer, K.K., Ward, B.D., Rao, S.M., Li, S.J., Hudetz, A.G., Propofol disrupts functional interactions between sensory and high-order processing of auditory verbal memory (2012) Hum Brain Mapp, 33, pp. 2487-2498
Dosenbach, N.U., Fair, D.A., Cohen, A.L., Schlaggar, B.L., Petersen, S.E., A dual-networks architecture of top-down control (2008) Trends Cogn Sci, 12 (3), pp. 99-105
Fassbender, C., Simoes-Franklin, C., Murphy, K., Hester, R., Meaney, J., Robertson, I.H., Garavan, H., The role of a right fronto-parietal network in cognitive control (2006) J Psychophysiol, 20 (4), pp. 286-296
Power, J.D., Cohen, A.L., Nelson, S.M., Wig, G.S., Barnes, K.A., Church, J.A., Vogel, A.C., Petersen, S.E., Functional network organization of the human brain (2011) Neuron, 72 (4), pp. 665-678
Guldenmund, P., Gantner, I.S., Baquero, K., Das, T., Demertzi, A., Boveroux, P., Bonhomme, V., Noirhomme, Q., Propofol-induced frontal cortex disconnection: a study of resting-state networks, total brain connectivity, and mean BOLD signal oscillation frequencies (2016) Brain Connect, 6 (3), pp. 225-237
Sadaghiani, S., Hesselmann, G., Kleinschmidt, A., Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection (2009) J Neurosci, 29 (42), pp. 13410-13417
Chadick, J.Z., Gazzaley, A., Differential coupling of visual cortex with default or frontal-parietal network based on goals (2011) Nat Neurosci, 14 (7), p. 830
Wallhausser-Franke, E., Tinnitus: distinguishing between subjectively perceived loudness and tinnitus-related distress (2012) PLoS One, 7 (4)
Vidal-Piñeiro, D., Decreased default mode network connectivity correlates with age-associated structural and cognitive changes (2014) Front Aging Neurosci, 6, p. 256
Washington, S.D., VanMeter, J.W., Anterior-posterior connectivity within the default mode network increases during maturation (2015) Int J Med Biol Front, 21 (2), p. 207
Ferreira, L.K., Regina, A.C., Kovacevic, N., Martin, M.D., Santos, P.P., Carneiro, C.D., Kerr, D.S., Busatto, G.F., Aging effects on whole-brain functional connectivity in adults free of cognitive and psychiatric disorders (2016) Cereb Cortex, 26 (9), pp. 3851-3865
Meyer, M., Luethi, M.S., Neff, P., Langer, N., Büchi, S., Disentangling Tinnitus Distress and Tinnitus presence by means of EEG power analysis (2014) Neural Plast, , (,),.,., https://doi.org/10.1155/2014/468546
Schlee, W., Kleinjung, T., Hiller, W., Goebel, G., Kolassa, I.T., Langguth, B., Does tinnitus distress depend on age of onset? (2011) PLoS One, 6 (11)
Brüggemann, P., Szczepek, A.J., Rose, M., McKenna, L., Olze, H., Mazurek, B., Impact of multiple factors on the degree of tinnitus distress (2016) Front Human Neurosci, 10, p. 341
Balkenhol, T., Wallhausser-Franke, E., Delb, W., Psychoacoustic tinnitus loudness and tinnitus-related distress show different associations with oscillatory brain activity (2013) PLoS One, 8 (1)
Tyler, R.S., Conrad-Armes, D., The determination of tinnitus loudness considering the effects of recruitment (1983) J Speech Hear Res, 26 (1), pp. 59-72
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