Eyes Closed vs. Eyes Open: Investigating Brain Activity Differences in Tinnitus Patients Using Multi-Channel Electroencephalography-A Preliminary Study
,
Abstract
Background and Aim: Tinnitus, the perception of sound without an external source, significantly affects the quality of life for millions worldwide. Although many studies have explored its pathophysiology and neural underpinnings using various methods during resting states, the influence of eye state on neural activity remains poorly understood. This study examined brain activity differences between eyes-closed and eyes-open resting states in individuals with chronic tinnitus.
Methods: In this cross-sectional study, twenty patients with chronic tinnitus underwent Electroencephalography (EEG) during both eyes-closed and eyes-open resting states. EEG power spectra, source localization, and functional connectivity were analyzed across eight frequency bands. Paired-sample t-test and Statistical Non-Parametric Mapping (SnPM) test compared activity between these conditions.
Results: Eyes-closed recordings showed decreased delta, theta, and gamma power, increased alpha 1 and alpha 2 power, and a complex beta pattern (increased beta 1, decreased beta 2 and beta 3) compared to eyes-open. Source localization analysis revealed greater activity in regions associated with memory, attention, and emotional processing during eyes-closed compared to eyes-open. Functional connectivity analysis indicated stronger connections between auditory and memory-related regions in eyes-closed compared to eyes-open.
Conclusions: This preliminary study demonstrated distinct EEG power spectra, source localization, and functional connectivity between eyes-closed and eyes-open states in chronic tinnitus patients, suggesting state-specific neural patterns. Findings highlight interactions of sensory, cognitive, and affective processes, potentially relevant to tinnitus. Further research with control groups and larger samples is needed to confirm tinnitus-specific effects and optimize EEG conditions for elucidating neural mechanisms and guiding targeted interventions.
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18. Foxe JJ, Snyder AC. The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention. Front Psychol. 2011 Jul 5;2:154. [DOI:10.3389/fpsyg.2011.00154]
19. Rosemann S, Rauschecker JP. Disruptions of default mode network and precuneus connectivity associated with cognitive dysfunctions in tinnitus. Sci Rep. 2023 ;13(1):5746. [DOI:10.1038/s41598-023-32599-0]
20. Moazami-Goudarzi M, Michels L, Weisz N, Jeanmonod D. Temporo-insular enhancement of EEG low and high frequencies in patients with chronic tinnitus. QEEG study of chronic tinnitus patients. BMC Neurosci. 2010;11:40. [DOI:10.1186/1471-2202-11-40]
21. Petro NM, Ott LR, Penhale SH, Rempe MP, Embury CM, Picci G, et al. Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development. Neuroimage. 2022; 258:119337. [DOI:10.1016/j.neuroimage.2022.11933]
22. Harmony T. The functional significance of delta oscillations in cognitive processing. Front Integr Neurosci. 2013; 7:83. [DOI:10.3389/fnint.2013.00083] [PMID]
23. Johnstone SJ, Jiang H, Sun L, Rogers JM, Valderrama J, Zhang D. Development of Frontal EEG differences between eyes-closed and eyes-open resting conditions in children: Data From a single-channel dry-sensor portable device. Clin EEG Neurosci. 2021; 52(4):235-45. [DOI:10.1177/1550059420946648] [PMID]
24. Villena-González M, Palacios-García I, Rodríguez E, López V. Beta oscillations distinguish between two forms of mental imagery while gamma and theta activity reflects auditory attention. Front Hum Neurosci. 2018; 12:389. [DOI:10.3389/fnhum.2018.00389] [PMID]
25. Milner R, Lewandowska M, Ganc M, Nikadon J, Niedziałek I, Jędrzejczak WW, Skarżyński H. Electrophysiological correlates of focused attention on low- and high-distressed tinnitus. Plos One. 2020; 15(8):e0236521. [DOI:10.1371/journal.pone.0236521] [PMID]
26. Strüber D, Herrmann CS. Gamma Activity in Sensory and Cognitive Processing. In: Gable PA, Miller MW, Bernat EM, editors. The Oxford Handbook of EEG Frequency. Oxford: Oxford University Press; 2022. [DOI:10.1093/oxfordhb/9780192898340.013.8]
27. Engelhard B, Ozeri N, Israel Z, Bergman H, Vaadia E. Inducing gamma oscillations and precise spike synchrony by operant conditioning via brain-machine interface. Neuron. 2013; 77(2):361-75. [DOI:10.1016/j.neuron.2012.11.015] [PMID]
28. Nguyen AT, Hetrick WP, O'Donnell BF, Brenner CA. Abnormal beta and gamma frequency neural oscillations mediate auditory sensory gating deficit in schizophrenia. J Psychiatr Res. 2020; 124:13-21. [DOI:10.1016/j.jpsychires.2020.01.014]
29. Hamel-Thibault A, Thénault F, Whittingstall K, Bernier PM. Delta-band oscillations in motor regions predict hand selection for reaching. Cereb Cortex. 2018; 28(2):574-84. [DOI:10.1093/cercor/bhw392]
30. Li M, Lu S, Zhong N. The Parahippocampal Cortex Mediates Contextual Associative Memory: Evidence from an fMRI Study. Biomed Res Int. 2016;2016:9860604. [DOI:10.1155/2016/9860604]
31. Collignon O, Vandewalle G, Voss P, Albouy G, Charbonneau G, Lassonde M, et al. Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans. Proc Natl Acad Sci U S A. 2011; 108(11):4435-40. [DOI:10.1073/pnas.1013928108]
32. Travis F, Parim N. Default mode network activation and Transcendental Meditation practice: Focused attention or automatic self-transcending? Brain Cogn. 2017; 111:86-94. [DOI:10.1016/j.bandc.2016.08.009]
33. Czornik M, Birbaumer N, Braun C, Hautzinger M, Wolpert S, Löwenheim H, et al. Neural substrates of tinnitus severity. Int J Psychophysiol. 2022; 181:40-49. [DOI:10.1016/j.ijpsycho.2022.08.009]
34. Palejwala AH, O'Connor KP, Milton CK, Anderson C, Pelargos P, Briggs RG, et al. Anatomy and white matter connections of the fusiform gyrus. Sci Rep. 2020; 10(1):13489. [DOI:10.1038/s41598-020-70410-6]
35. Spagna A, Hajhajate D, Liu J, Bartolomeo P. Visual mental imagery engages the left fusiform gyrus, but not the early visual cortex: A meta-analysis of neuroimaging evidence. Neurosci Biobehav Rev. 2021; 122:201-17. [DOI:10.1016/j.neubiorev.2020.12.029] [PMID]
36. Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014; 137(Pt 1):12-32. [DOI:10.1093/brain/awt162]
37. Zimmerman BJ, Schmidt SA, Khan RA, Tai Y, Shahsavarani S, Husain FT. Decreased resting perfusion in precuneus and posterior cingulate cortex predicts tinnitus severity. Curr Res Neurobiol. 2021; 2:100010. [DOI:10.1016/j.crneur.2021.100010] [PMID]
38. Costumero V, Bueichekú E, Adrián-Ventura J, Ávila C. Opening or closing eyes at rest modulates the functional connectivity of V1 with default and salience networks. Sci Rep. 2020; 10(1):9137. [DOI:10.1038/s41598-020-66100-y]
39. Molholm S, Sehatpour P, Mehta AD, Shpaner M, Gomez-Ramirez M, Ortigue S, et al. Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings. J Neurophysiol. 2006; 96(2):721-9. [DOI:10.1152/jn.00285.2006]
40. Klimesch W. α-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci. 2012; 16(12):606-17. [DOI:10.1016/j.tics.2012.10.007]
41. Schmidt SA, Akrofi K, Carpenter-Thompson JR, Husain FT. Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. Plos One. 2013; 8(10):e76488. [DOI:10.1371/journal.pone.0076488]
42. Berger JI, Billig AJ, Sedley W, Kumar S, Griffiths TD, Gander PE. What is the role of the hippocampus and parahippocampal gyrus in the persistence of tinnitus? Hum Brain Mapp. 2024; 45(3):e26627. [DOI:10.1002/hbm.26627]
43. Kuusinen V, Cesnaite E, Peräkylä J, Ogawa KH, Hartikainen KM. orbitofrontal lesion alters brain dynamics of emotion-attention and emotion-cognitive control interaction in humans. Front Hum Neurosci. 2018; 12:437. [DOI:10.3389/fnhum.2018.00437] [PMID]
44. Goddard CA, Sridharan D, Huguenard JR, Knudsen EI. Gamma oscillations are generated locally in an attention-related midbrain network. Neuron. 2012; 73(3):567-80. [DOI:10.1016/j.neuron.2011.11.028]
45. Chen YC, Liu S, Lv H, Bo F, Feng Y, Chen H, et al. Abnormal resting-state functional connectivity of the anterior cingulate cortex in unilateral chronic tinnitus patients. Front Neurosci. 2018; 12:9. [DOI:10.3389/fnins.2018.00009]
2. Hamed SA, Attiah FA, Fawzy M, Azzam M. Evaluation of chronic idiopathic tinnitus and its psychosocial triggers. World J Clin Cases. 2023; 11(14):3211-23. [DOI: 10.12998/wjcc.v11.i14.3211]
3. Vanneste S, Plazier M, der Loo Ev, de Heyning PV, Congedo M, De Ridder D. The neural correlates of tinnitus-related distress. Neuroimage. 2010;52(2):470-80. [DOI:10.1016/j.neuroimage.2010.04.029]
4. Adjamian P, Hall DA, Palmer AR, Allan TW, Langers DR. Neuroanatomical abnormalities in chronic tinnitus in the human brain. Neurosci Biobehav Rev. 2014; 45:119-33. [DOI:10.1016/j.neubiorev.2014.05.013]
5. Mohsen S, Mahmoudian S, Talebian S, Pourbakht A. Multisite transcranial Random Noise Stimulation (tRNS) modulates the distress network activity and oscillatory powers in subjects with chronic tinnitus. J Clin Neurosci. 2019; 67:178-184. [DOI:10.1016/j.jocn.2019.06.033]
6. De Ridder D, Friston K, Sedley W, Vanneste S. A parahippocampal-sensory Bayesian vicious circle generates pain or tinnitus: A source-localized EEG study. Brain Commun. 2023; 5(3):fcad132. [DOI:10.1093/braincomms/fcad132]
7. Husain FT, Schmidt SA. Using resting state functional connectivity to unravel networks of tinnitus. Hear Res. 2014;307:153-62. [DOI:10.1016/j.heares.2013.07.010]
8. Lan L, Li J, Chen Y, Chen W, Li W, Zhao F, et al. Alterations of brain activity and functional connectivity in transition from acute to chronic tinnitus. Hum Brain Mapp. 2021; 42(2):485-94. [DOI:10.1002/hbm.25238]
9. Vanneste S, De Ridder D. Stress-related functional connectivity changes between auditory cortex and cingulate in tinnitus. Brain Connect. 2015; 5(6):371-83. [DOI:10.1089/brain.2014.0255]
10. Agcaoglu O, Wilson TW, Wang YP, Stephen JM, Calhoun VD. Dynamic Resting-State Connectivity Differences in Eyes Open Versus Eyes Closed Conditions. Brain Connect. 2020 Nov;10(9):504-519. [DOI:10.1089/brain.2020.0768]
11. Barry RJ, Clarke AR, Johnstone SJ, Magee CA, Rushby JA. EEG differences between eyes-closed and eyes-open resting conditions. Clin Neurophysiol. 2007; 118(12):2765-73. [DOI:10.1016/j.clinph.2007.07.028]
12. Isler JR, Pini N, Lucchini M, Shuffrey LC, Morales S, Bowers ME, et al. Longitudinal characterization of EEG power spectra during eyes open and eyes closed conditions in children. Psychophysiology. 2023; 60(1):e14158. [DOI:10.1111/psyp.14158]
13. Chang SD, Kuo PC, Zilles K, Duong TQ, Eickhoff SB, Huang ACW, et al. Brain reactions to opening and closing the eyes: Salivary cortisol and functional connectivity. Brain Topogr. 2022; 35(4):375-97. [DOI:10.1007/s10548-022-00897-x]
14. Han J, Zhou L, Wu H, Huang Y, Qiu M, Huang L, Lee C, Lane TJ, Qin P. Eyes-Open and Eyes-Closed Resting State Network Connectivity Differences. Brain Sci. 2023; 13(1):122. [DOI:10.3390/brainsci13010122]
15. Alonso-Valerdi LM, Ibarra-Zarate DI, Tavira-Sánchez FJ, Ramírez-Mendoza RA, Recuero M. Electroencephalographic evaluation of acoustic therapies for the treatment of chronic and refractory tinnitus. BMC Ear Nose Throat Disord. 2017; 17:9. [DOI:10.1186/s12901-017-0042-z]
16. Hu J, Cui J, Xu JJ, Yin X, Wu Y, Qi J. The Neural Mechanisms of Tinnitus: A Perspective From Functional Magnetic Resonance Imaging. Front Neurosci. 2021; 15:621145. [DOI: 10.3389/fnins.2021.621145]
17. Kok TE, Domingo D, Hassan J, Vuong A, Hordacre B, Clark C, et al. Resting-state Networks in Tinnitus : A Scoping Review. Clin Neuroradiol. 2022 Dec;32(4):903-22. [DOI:10.1007/s00062-022-01170-1]
18. Foxe JJ, Snyder AC. The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention. Front Psychol. 2011 Jul 5;2:154. [DOI:10.3389/fpsyg.2011.00154]
19. Rosemann S, Rauschecker JP. Disruptions of default mode network and precuneus connectivity associated with cognitive dysfunctions in tinnitus. Sci Rep. 2023 ;13(1):5746. [DOI:10.1038/s41598-023-32599-0]
20. Moazami-Goudarzi M, Michels L, Weisz N, Jeanmonod D. Temporo-insular enhancement of EEG low and high frequencies in patients with chronic tinnitus. QEEG study of chronic tinnitus patients. BMC Neurosci. 2010;11:40. [DOI:10.1186/1471-2202-11-40]
21. Petro NM, Ott LR, Penhale SH, Rempe MP, Embury CM, Picci G, et al. Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development. Neuroimage. 2022; 258:119337. [DOI:10.1016/j.neuroimage.2022.11933]
22. Harmony T. The functional significance of delta oscillations in cognitive processing. Front Integr Neurosci. 2013; 7:83. [DOI:10.3389/fnint.2013.00083] [PMID]
23. Johnstone SJ, Jiang H, Sun L, Rogers JM, Valderrama J, Zhang D. Development of Frontal EEG differences between eyes-closed and eyes-open resting conditions in children: Data From a single-channel dry-sensor portable device. Clin EEG Neurosci. 2021; 52(4):235-45. [DOI:10.1177/1550059420946648] [PMID]
24. Villena-González M, Palacios-García I, Rodríguez E, López V. Beta oscillations distinguish between two forms of mental imagery while gamma and theta activity reflects auditory attention. Front Hum Neurosci. 2018; 12:389. [DOI:10.3389/fnhum.2018.00389] [PMID]
25. Milner R, Lewandowska M, Ganc M, Nikadon J, Niedziałek I, Jędrzejczak WW, Skarżyński H. Electrophysiological correlates of focused attention on low- and high-distressed tinnitus. Plos One. 2020; 15(8):e0236521. [DOI:10.1371/journal.pone.0236521] [PMID]
26. Strüber D, Herrmann CS. Gamma Activity in Sensory and Cognitive Processing. In: Gable PA, Miller MW, Bernat EM, editors. The Oxford Handbook of EEG Frequency. Oxford: Oxford University Press; 2022. [DOI:10.1093/oxfordhb/9780192898340.013.8]
27. Engelhard B, Ozeri N, Israel Z, Bergman H, Vaadia E. Inducing gamma oscillations and precise spike synchrony by operant conditioning via brain-machine interface. Neuron. 2013; 77(2):361-75. [DOI:10.1016/j.neuron.2012.11.015] [PMID]
28. Nguyen AT, Hetrick WP, O'Donnell BF, Brenner CA. Abnormal beta and gamma frequency neural oscillations mediate auditory sensory gating deficit in schizophrenia. J Psychiatr Res. 2020; 124:13-21. [DOI:10.1016/j.jpsychires.2020.01.014]
29. Hamel-Thibault A, Thénault F, Whittingstall K, Bernier PM. Delta-band oscillations in motor regions predict hand selection for reaching. Cereb Cortex. 2018; 28(2):574-84. [DOI:10.1093/cercor/bhw392]
30. Li M, Lu S, Zhong N. The Parahippocampal Cortex Mediates Contextual Associative Memory: Evidence from an fMRI Study. Biomed Res Int. 2016;2016:9860604. [DOI:10.1155/2016/9860604]
31. Collignon O, Vandewalle G, Voss P, Albouy G, Charbonneau G, Lassonde M, et al. Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans. Proc Natl Acad Sci U S A. 2011; 108(11):4435-40. [DOI:10.1073/pnas.1013928108]
32. Travis F, Parim N. Default mode network activation and Transcendental Meditation practice: Focused attention or automatic self-transcending? Brain Cogn. 2017; 111:86-94. [DOI:10.1016/j.bandc.2016.08.009]
33. Czornik M, Birbaumer N, Braun C, Hautzinger M, Wolpert S, Löwenheim H, et al. Neural substrates of tinnitus severity. Int J Psychophysiol. 2022; 181:40-49. [DOI:10.1016/j.ijpsycho.2022.08.009]
34. Palejwala AH, O'Connor KP, Milton CK, Anderson C, Pelargos P, Briggs RG, et al. Anatomy and white matter connections of the fusiform gyrus. Sci Rep. 2020; 10(1):13489. [DOI:10.1038/s41598-020-70410-6]
35. Spagna A, Hajhajate D, Liu J, Bartolomeo P. Visual mental imagery engages the left fusiform gyrus, but not the early visual cortex: A meta-analysis of neuroimaging evidence. Neurosci Biobehav Rev. 2021; 122:201-17. [DOI:10.1016/j.neubiorev.2020.12.029] [PMID]
36. Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014; 137(Pt 1):12-32. [DOI:10.1093/brain/awt162]
37. Zimmerman BJ, Schmidt SA, Khan RA, Tai Y, Shahsavarani S, Husain FT. Decreased resting perfusion in precuneus and posterior cingulate cortex predicts tinnitus severity. Curr Res Neurobiol. 2021; 2:100010. [DOI:10.1016/j.crneur.2021.100010] [PMID]
38. Costumero V, Bueichekú E, Adrián-Ventura J, Ávila C. Opening or closing eyes at rest modulates the functional connectivity of V1 with default and salience networks. Sci Rep. 2020; 10(1):9137. [DOI:10.1038/s41598-020-66100-y]
39. Molholm S, Sehatpour P, Mehta AD, Shpaner M, Gomez-Ramirez M, Ortigue S, et al. Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings. J Neurophysiol. 2006; 96(2):721-9. [DOI:10.1152/jn.00285.2006]
40. Klimesch W. α-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci. 2012; 16(12):606-17. [DOI:10.1016/j.tics.2012.10.007]
41. Schmidt SA, Akrofi K, Carpenter-Thompson JR, Husain FT. Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. Plos One. 2013; 8(10):e76488. [DOI:10.1371/journal.pone.0076488]
42. Berger JI, Billig AJ, Sedley W, Kumar S, Griffiths TD, Gander PE. What is the role of the hippocampus and parahippocampal gyrus in the persistence of tinnitus? Hum Brain Mapp. 2024; 45(3):e26627. [DOI:10.1002/hbm.26627]
43. Kuusinen V, Cesnaite E, Peräkylä J, Ogawa KH, Hartikainen KM. orbitofrontal lesion alters brain dynamics of emotion-attention and emotion-cognitive control interaction in humans. Front Hum Neurosci. 2018; 12:437. [DOI:10.3389/fnhum.2018.00437] [PMID]
44. Goddard CA, Sridharan D, Huguenard JR, Knudsen EI. Gamma oscillations are generated locally in an attention-related midbrain network. Neuron. 2012; 73(3):567-80. [DOI:10.1016/j.neuron.2011.11.028]
45. Chen YC, Liu S, Lv H, Bo F, Feng Y, Chen H, et al. Abnormal resting-state functional connectivity of the anterior cingulate cortex in unilateral chronic tinnitus patients. Front Neurosci. 2018; 12:9. [DOI:10.3389/fnins.2018.00009]
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How to Cite
1.
Nazeri S, Fatahi F, Talebian S, Yazdani N. Eyes Closed vs. Eyes Open: Investigating Brain Activity Differences in Tinnitus Patients Using Multi-Channel Electroencephalography-A Preliminary Study. Aud Vestib Res. 2025;.
