Investigating sensitivity to multi-domain prediction errors in chronic auditory phantom perception.
Deafferentation
Predictive coding
Sensory prediction error
Tinnitus
Visual domain
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 05 2024
14 05 2024
Historique:
received:
04
03
2024
accepted:
29
04
2024
medline:
15
5
2024
pubmed:
15
5
2024
entrez:
14
5
2024
Statut:
epublish
Résumé
The perception of a continuous phantom in a sensory domain in the absence of an external stimulus is explained as a maladaptive compensation of aberrant predictive coding, a proposed unified theory of brain functioning. If this were true, these changes would occur not only in the domain of the phantom percept but in other sensory domains as well. We confirm this hypothesis by using tinnitus (continuous phantom sound) as a model and probe the predictive coding mechanism using the established local-global oddball paradigm in both the auditory and visual domains. We observe that tinnitus patients are sensitive to changes in predictive coding not only in the auditory but also in the visual domain. We report changes in well-established components of event-related EEG such as the mismatch negativity. Furthermore, deviations in stimulus characteristics were correlated with the subjective tinnitus distress. These results provide an empirical confirmation that aberrant perceptions are a symptom of a higher-order systemic disorder transcending the domain of the percept.
Identifiants
pubmed: 38744906
doi: 10.1038/s41598-024-61045-y
pii: 10.1038/s41598-024-61045-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
11036Subventions
Organisme : Irish Research Council (An Chomhairle um Thaighde in Éirinn)
ID : GOIPD/2020/663
Organisme : Royal Irish Academy (Acadamh Ríoga na hÉireann)
ID : Charlemont Grant 2021
Organisme : Ministry of Education and Science of the Russian Federation (Minobrnauka)
ID : State Assignment
Informations de copyright
© 2024. The Author(s).
Références
Rao, R. P. & Ballard, D. H. Predictive coding in the visual cortex: A functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2(1), 79–87 (1999).
pubmed: 10195184
doi: 10.1038/4580
Hullfish, J., Sedley, W. & Vanneste, S. Prediction and perception: Insights for (and from) tinnitus. Neurosci. Biobehav. Rev. 102, 1–12 (2019).
pubmed: 30998951
doi: 10.1016/j.neubiorev.2019.04.008
Mohan, A. & Vanneste, S. Adaptive and maladaptive neural compensatory consequences of sensory deprivation—from a phantom percept perspective. Prog. Neurobiol. 153, 1–17 (2017).
pubmed: 28408150
doi: 10.1016/j.pneurobio.2017.03.010
Baguley, D., McFerran, D. & Hall, D. Tinnitus. The Lancet 382(9904), 1600–1607 (2013).
doi: 10.1016/S0140-6736(13)60142-7
Cohen, S. P., Vase, L. & Hooten, W. M. Chronic pain: An update on burden, best practices, and new advances. The Lancet 397(10289), 2082–2097 (2021).
doi: 10.1016/S0140-6736(21)00393-7
Grouios, G. Phantom smelling. Percept. Motor Skills 94(3), 841–850 (2002).
pubmed: 12081289
doi: 10.2466/pms.2002.94.3.841
Maheswaran, T. et al. Gustatory dysfunction. J. Pharm. Bioallied Sci. 6(Suppl 1), S30 (2014).
pubmed: 25210380
pmcid: 4157276
doi: 10.4103/0975-7406.137257
Schadlu, A. P., Schadlu, R. & Shepherd, J. B. Charles Bonnet syndrome: A review. Curr. Opin. Ophthalmol. 20(3), 219–222 (2009).
pubmed: 19349864
doi: 10.1097/ICU.0b013e328329b643
Jansen, E. et al. Noise induced hearing loss and other hearing complaints among musicians of symphony orchestras. Int. Arch. Occup. Env. Health 82(2), 153–164 (2009).
doi: 10.1007/s00420-008-0317-1
Baron, R. Mechanisms of disease: Neuropathic pain—a clinical perspective. Nat. Clin. Pract. Neurol. 2(2), 95–106 (2006).
pubmed: 16932531
doi: 10.1038/ncpneuro0113
Wrobel, B. B. & Leopold, D. A. Clinical assessment of patients with smell and taste disorders. Otolaryngol. Clin. N. Am. 37(6), 1127–1142 (2004).
doi: 10.1016/j.otc.2004.06.010
Kester, E. M. Charles Bonnet syndrome: Case presentation and literature review. Optometry J. Am. Optometr. Assoc. 80(7), 360–366 (2009).
doi: 10.1016/j.optm.2008.10.017
Eggermont, J. Tinnitus: Some thoughts about its origin. J. Laryngol. Otol. 98(S9), 31–37 (1984).
doi: 10.1017/S1755146300090089
De Ridder, D., Vanneste, S. & Freeman, W. The Bayesian brain: Phantom percepts resolve sensory uncertainty. Neurosci. Biobehav. Rev. 44, 4–15 (2014).
pubmed: 22516669
doi: 10.1016/j.neubiorev.2012.04.001
Sedley, W. et al. An integrative tinnitus model based on sensory precision. Trends Neurosci. 39(12), 799–812 (2016).
pubmed: 27871729
pmcid: 5152595
doi: 10.1016/j.tins.2016.10.004
Yaribeygi, H. et al. The impact of stress on body function: A review. Excli j 16, 1057–1072 (2017).
pubmed: 28900385
pmcid: 5579396
Patil, J. D. et al. The association between stress, emotional states, and tinnitus: A mini-review. Front. Aging Neurosci. 2023, 15 (2023).
Partyka, M. et al. Phantom auditory perception (tinnitus) is characterised by stronger anticipatory auditory predictions. BioRxiv 2019, 869842 (2019).
Sedley, W. et al. Exposing pathological sensory predictions in tinnitus using auditory intensity deviant evoked responses. J. Neurosci. 39(50), 10096 (2019).
pubmed: 31699888
pmcid: 6978936
doi: 10.1523/JNEUROSCI.1308-19.2019
Mohan, A. et al. Predisposition to domain-wide maladaptive changes in predictive coding in auditory phantom perception. NeuroImage 2021, 118813 (2021).
Bekinschtein, T. A. et al. Neural signature of the conscious processing of auditory regularities. Proc. Natl. Acad. Sci. 106(5), 1672–1677 (2009).
pubmed: 19164526
pmcid: 2635770
doi: 10.1073/pnas.0809667106
Chao, Z. C. et al. Large-scale cortical networks for hierarchical prediction and prediction error in the primate brain. Neuron 100(5), 1252–1266 (2018).
pubmed: 30482692
doi: 10.1016/j.neuron.2018.10.004
Wacongne, C. et al. Evidence for a hierarchy of predictions and prediction errors in human cortex. Proc. Natl. Acad. Sci. 108(51), 20754–20759 (2011).
pubmed: 22147913
pmcid: 3251061
doi: 10.1073/pnas.1117807108
Näätänen, R. et al. Attention and mismatch negativity. Psychophysiology 30(5), 436–450 (1993).
pubmed: 8416070
doi: 10.1111/j.1469-8986.1993.tb02067.x
Polich, J. Updating P300: An integrative theory of P3a and P3b. Clin. Neurophysiol. 118(10), 2128–2148 (2007).
pubmed: 17573239
pmcid: 2715154
doi: 10.1016/j.clinph.2007.04.019
Garrido, M. I. et al. Dynamic causal modeling of the response to frequency deviants. J. Neurophysiol. 101(5), 2620–2631 (2009).
pubmed: 19261714
pmcid: 2681422
doi: 10.1152/jn.90291.2008
Garrido, M. I. et al. Evoked brain responses are generated by feedback loops. Proc. Natl. Acad. Sci. 104(52), 20961–20966 (2007).
pubmed: 18087046
pmcid: 2409249
doi: 10.1073/pnas.0706274105
Wacongne, C., Changeux, J.-P. & Dehaene, S. A neuronal model of predictive coding accounting for the mismatch negativity. J. Neurosci. 32(11), 3665–3678 (2012).
pubmed: 22423089
pmcid: 6703454
doi: 10.1523/JNEUROSCI.5003-11.2012
May, P. J. & Tiitinen, H. Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. Psychophysiology 47(1), 66–122 (2010).
pubmed: 19686538
doi: 10.1111/j.1469-8986.2009.00856.x
Garrido, M. I. et al. The mismatch negativity: A review of underlying mechanisms. Clin. Neurophysiol. 120(3), 453–463 (2009).
pubmed: 19181570
pmcid: 2671031
doi: 10.1016/j.clinph.2008.11.029
Stefanics, G., Kremláček, J. & Czigler, I. Visual mismatch negativity: A predictive coding view. Front. Hum. Neurosci. 8, 666 (2014).
pubmed: 25278859
pmcid: 4165279
doi: 10.3389/fnhum.2014.00666
Nakao, M. et al. Somatosensory amplification and its relationship to somatosensory, auditory, and visual evoked and event-related potentials (P300). Neurosci. Lett. 415(2), 185–189 (2007).
pubmed: 17267120
doi: 10.1016/j.neulet.2007.01.021
Mohan, A. et al. Predisposition to domain-wide maladaptive changes in predictive coding in auditory phantom perception. NeuroImage 248, 11418 (2021).
Mathers, C., Smith, A. & Concha, M. Global burden of hearing loss in the year 2000. Glob. Burden Dis. 18(4), 1–30 (2000).
Allard, R. & Faubert, J. The noisy-bit method for digital displays: Converting a 256 luminance resolution into a continuous resolution. Behav. Res. Methods 40(3), 735–743 (2008).
pubmed: 18697669
doi: 10.3758/BRM.40.3.735
Oostenveld, R. et al. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 156869 (2011).
pubmed: 21253357
doi: 10.1155/2011/156869
El-Minawi, M. S. et al. Does changes in mismatch negativity after tinnitus retraining therapy using tinnitus pitch as deviant stimulus, reflect subjective improvement in tinnitus handicap?. Hear. Balance Commun. 16(3), 182–196 (2018).
doi: 10.1080/21695717.2018.1500003
Asadpour, A., Jahed, M. & Mahmoudian, S. Aberrant frequency related change-detection activity in chronic tinnitus. Front. Neurosci. 2020, 14 (2020).
Sendesen, E., Erbil, N. & Türkyılmaz, M. D. The mismatch negativity responses of individuals with tinnitus with normal extended high-frequency hearing—is it possible to use mismatch negativity in the evaluation of tinnitus?. Eur. Arch. Oto-Rhino-Laryngol. 2021, 1–10 (2021).
Weisz, N. et al. Abnormal auditory mismatch response in tinnitus sufferers with high-frequency hearing loss is associated with subjective distress level. BMC Neurosci. 5(1), 1–9 (2004).
doi: 10.1186/1471-2202-5-8
Umbricht, D. & Krljes, S. Mismatch negativity in schizophrenia: A meta-analysis. Schizophrenia Res. 76(1), 1–23 (2005).
doi: 10.1016/j.schres.2004.12.002
Fisher, D. J., Labelle, A. & Knott, V. J. The right profile: Mismatch negativity in schizophrenia with and without auditory hallucinations as measured by a multi-feature paradigm. Clin. Neurophysiol. 119(4), 909–921 (2008).
pubmed: 18261954
doi: 10.1016/j.clinph.2007.12.005
Light, G. A., Swerdlow, N. R. & Braff, D. L. Preattentive sensory processing as indexed by the MMN and P3a brain responses is associated with cognitive and psychosocial functioning in healthy adults. J. Cogn. Neurosci. 19(10), 1624–1632 (2007).
pubmed: 18271737
pmcid: 2562660
doi: 10.1162/jocn.2007.19.10.1624
De Ridder, D. et al. Tinnitus and the triple network model: A perspective. Clin. Exp. Otorhinolaryngol. 15(3), 205–212 (2022).
pubmed: 35835548
pmcid: 9441510
doi: 10.21053/ceo.2022.00815
Roberts, L. E., Husain, F. T. & Eggermont, J. J. Role of attention in the generation and modulation of tinnitus. Neurosci. Biobehav. Rev. 37(8), 1754–1773 (2013).
pubmed: 23876286
doi: 10.1016/j.neubiorev.2013.07.007
Marian, V., Hayakawa, S. & Schroeder, S. R. Cross-modal interaction between auditory and visual input impacts memory retrieval. Front. Neurosci. 15, 661477 (2021).
pubmed: 34381328
pmcid: 8350348
doi: 10.3389/fnins.2021.661477
Eckert, M. A. et al. A cross-modal system linking primary auditory and visual cortices: Evidence from intrinsic fMRI connectivity analysis. Hum. Brain Mapp. 29(7), 848–857 (2008).
pubmed: 18412133
pmcid: 2605422
doi: 10.1002/hbm.20560
Chen, L.-C., Puschmann, S. & Debener, S. Increased cross-modal functional connectivity in cochlear implant users. Sci. Rep. 7(1), 10043 (2017).
pubmed: 28855675
pmcid: 5577186
doi: 10.1038/s41598-017-10792-2
Coad, M. L. et al. Characteristics of patients with gaze-evoked tinnitus. Otol. Neurotol. 22(5), 650–654 (2001).
pubmed: 11568674
doi: 10.1097/00129492-200109000-00016
Li, Z. et al. Eyes and ears: Cross-modal interference of tinnitus on visual processing. Front. Psychol. 9, 1779 (2018).
pubmed: 30319490
pmcid: 6166004
doi: 10.3389/fpsyg.2018.01779
Amaral, A. A. & Langers, D. R. M. Tinnitus-related abnormalities in visual and salience networks during a one-back task with distractors. Hear. Res. 326, 15–29 (2015).
pubmed: 25843940
doi: 10.1016/j.heares.2015.03.006
Ueyama, T. et al. Brain regions responsible for tinnitus distress and loudness: A resting-state FMRI study. PLoS One 8(6), e67778 (2013).
pubmed: 23825684
pmcid: 3692468
doi: 10.1371/journal.pone.0067778
Vanneste, S. et al. The neural correlates of tinnitus-related distress. NeuroImage 52(2), 470–480 (2010).
pubmed: 20417285
doi: 10.1016/j.neuroimage.2010.04.029
Zeng, F. G. Tinnitus and hyperacusis: Central noise, gain and variance. Curr. Opin. Physiol. 18, 123–129 (2020).
pubmed: 33299958
pmcid: 7720792
doi: 10.1016/j.cophys.2020.10.009
Mohan, A. et al. Effective connectivity analysis of inter- and intramodular hubs in phantom sound perception—identifying the core distress network. Brain Imaging Behav. 14(1), 289–307 (2020).
pubmed: 30443893
doi: 10.1007/s11682-018-9989-7
Mohan, A. et al. Distress-dependent temporal variability of regions encoding domain-specific and domain-general behavioral manifestations of phantom percepts. Eur. J. Neurosci. 48(2), 1743–1764 (2018).
pubmed: 29888410
doi: 10.1111/ejn.13988
Vanneste, S., Congedo, M. & De Ridder, D. Pinpointing a highly specific pathological functional connection that turns phantom sound into distress. Cerebral Cortex 24(9), 2268–2282 (2014).
pubmed: 23632885
doi: 10.1093/cercor/bht068