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Loss of alpha power is related to increased gamma synchronization—A marker of reduced inhibition in tinnitus?

Tinnitus is the perception of sound in the absence of any external auditory stimulus. Based on previous research we have proposed a framework which postulates that the reduction of ongoing inhibitory alpha activity in tinnitus subjects favors a
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  Neuroscience Letters 453 (2009) 225–228 Contents lists available at ScienceDirect Neuroscience Letters  journal homepage: www.elsevier.com/locate/neulet Loss of alpha power is related to increased gamma synchronization—A markerof reduced inhibition in tinnitus? Isabel Lorenz ∗ , Nadia Müller, Winfried Schlee, Thomas Hartmann, Nathan Weisz University of Konstanz, Konstanz, Germany a r t i c l e i n f o  Article history: Received 11 June 2008Received in revised form 21 October 2008Accepted 18 February 2009 Keywords: TinnitusOscillatory brain activityAlphaGammaMagnetoencephalography a b s t r a c t Tinnitus is the perception of sound in the absence of any external auditory stimulus. Based on previousresearchwehaveproposedaframeworkwhichpostulatesthatthereductionofongoinginhibitoryalphaactivityintinnitussubjectsfavorsasynchronizationofneuronsinthegammafrequencyrangewhileinarestingstate.Inthepresentworkwearevalidatingtheexistenceofaninverserelationshipbetweenaudi-tory gamma and alpha activity in tinnitus and control subjects using Magnetoencephalography. Tinnitussubjects exhibited a significantly steeper slope of the regression line compared to controls, presumablybecauseagreaternumberofsubjectsconcurrentlyexhibitedlowalphaandhighgammapower.Therefore,the role of the alpha–gamma pattern is discussed regarding its possible implication for the generation of tinnitus.© 2009 Elsevier Ireland Ltd. All rights reserved. Tinnitus is the subjective perception of sound (e.g., a ringing orhissing noise) in the absence of any external stimulus. The con-dition affects approximately 5–15% of the population in westernsocieties [6] and to date the underlying neuronal mechanisms of  tinnitus are still not completely understood. One likely trigger of tinnitus is damage to the peripheral hearing system. This damageleads to aberrant central auditory activity, i.e. an overall increasein the firing of neurons, especially in the dorsal cochlear nucleus[12], the inferior colliculus, the primary and the secondary audi-tory cortex [6]. Furthermore, it has been shown that populations of neurons with an increased firing rate locally synchronize theiractivity [21].In previous research using Magnetoencephalography (MEG),our group demonstrated abnormalities in the power spectrumof chronic tinnitus patients while in the resting state [32,33].These changes were characterized by a noticeable reduction of power in the alpha (8–12Hz) frequency band and a concomitantenhancementinthedelta(0.5–4Hz)aswellasthegamma(>30Hz)frequency range in temporal cortical regions. To further examinethese abnormalities we are going to concentrate on the interactionof alpha and gamma power in the present work.In recordings of spontaneous activity, alpha usually domi-nates the power spectrum since alpha rhythms can be foundin virtually all sensory and motor areas while subjects are at ∗ Corresponding author at: Department of Psychology, University of Konstanz,P.O. Box D25, 78458 Konstanz, Germany. Tel.: +49 7531 88 3571;fax: +49 7531 88 4601. E-mail address:  Isabel.Lorenz@uni-konstanz.de (I. Lorenz). rest [2]. However, this does not mean that alpha rhythms are the neural code of ‘doing nothing’ as the frequently-used term‘idling-rhythm’ may imply. Based on studies of event-relatedalpha reductions (‘Event-Related Desynchronization’; ERD) andenhancements (‘Event-Related Synchronization’; ERS) Klimeschet al. [15] hypothesized that oscillations in the alpha frequencyrange emerge from rhythmical fluctuations of inhibitory neurons.This notion finds support in recent studies which combine Elec-troencephalography (EEG) with Transcranial Magnetic Stimulation(TMS) [10,14,23].Neuronal activity in the gamma frequency range, however, hasbeen demonstrated to be associated with almost all categories of higher-order cognitive functions such as feature specification andcognitive binding [22,28,9]. Gamma activity has been associated with synchronization of firing within [8] as well as between neu- ronal cell-assemblies [27].The existence of an antagonistic nature of alpha and gammarhythms has been indicated, for example, by fMRI studies relatingsignalchangesinbloodoxygenlevel-dependent(BOLD)tochangesin electrophysiological responses [18,16]: Gamma activity is posi- tively correlated with the BOLD signal [18], whereas alpha activity exhibits a negative relationship [16].From a clinical perspective, enhanced neuronal activity in thegamma frequency range in the  resting state  has been linked topositive symptoms in some neuropsychiatric disorders, includingtinnitus [17].With the  Synchronization-by-Loss-of-Inhibition-Model  (SLIM)[31] we recently proposed a framework to explain the observedoscillatory changes in tinnitus and to derive scientific as well asclinicalpredictions.Thismodelessentiallyarguesthatinputdepri- 0304-3940/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved.doi:10.1016/j.neulet.2009.02.028  226  I. Lorenz et al. / Neuroscience Letters 453 (2009) 225–228 vation (caused by deafferentation due to hearing loss) leads toreduced activity and therefore to an enhancement of delta poweralong the tonotopic axis. In addition to a suppression of excitatoryneuron activity, the activity of inhibitory neurons, whose impactnormallyisreflectedasalphaactivity[15,19,24],isalsosuppressed. The exact srcin of alpha is still a matter of ongoing debate, yetrecentfindings[3]indicatethatatleastsomeformsofalphaemerge fromtheintracorticalinteractionsofneurons,ratherthanjustbeingpassivelydrivenbythalamicafferents.Theassumed‘releaseofinhi-bition’, may indicate a spontaneous synchronization of firing of excitatory neurons in circumscribed regions of the tonotopic axis.Increased synchronized neuronal activity is then reflected withinthe gamma frequency range. Since synchronized activity is cru-cial for a coherent percept, abnormally enhanced gamma activityin the auditory cortex might be a necessary requirement of thesound perception in tinnitus [33]. Chronification of tinnitus could result from longer lasting synchronous firing, leading to enhancedsynaptic efficacy within a neuronal cell assembly via Hebbianmechanisms.If dominant resting alpha activity reflects a mechanism thatsuppressesundesirable‘spontaneous’high-frequencysynchroniza-tion, as postulated by SLIM [31], then one prediction, which has been untested to date, would be that levels of auditory alpha andgamma activity are inversely related. The purpose of the presentMEG study was to test this hypothesis of an inverse relationshipbetween alpha and gamma activity in tinnitus and control sub- jects. Furthermore, the influence of tinnitus on such a relationshipis examined more closely.Twenty-sixsubjectssufferingfromchronictinnitusparticipatedinthestudy(20male,6female).Themeanagewas45years(range:20–65 years); the mean tinnitus duration 6.75 years ( ± 1.01). Sub- jectswererecruitedviaadvertisementsinthelocalnewspaperandflyers at the University of Konstanz. Nine subjects reported dom-inant left, 10 bilaterally equal, and 7 dominant right lateralizedtinnitus. Tinnitus distress was assessed using the German versionof the Tinnitus Questionnaire [7]. The average distress score was 27.48( ± 3.54),correspondingtomilddistress.Twenty-onesubjectswithouttinnitusorotherhearingdisorderservedasacontrolgroup(16males,5females,meanage:35years;range:23–78years).NoneofthesubjectshasparticipatedinanMEGstudybefore.Theexper-iment has been conducted in accordance with the declaration of Helsinki and with adequate understanding and written informedconsent of the subjects.Five minutes of MEG under a resting condition were recorded(sampling rate: 678.17, 0.1–200Hz band-pass) using a 148-channelwhole-headmagnetometer(Magnes2500WH;4-DNeuroimaging,San Diego, CA) in a magnetically shielded chamber (Vakuum-schmelze, Hanau, Germany). Participants lay in a supine positionandwererequestedtokeepeyesopenandtofocusonafixedpointontheceiling.Fourelectrodeswereusedtorecordeyemovements(electrooculogramm, EOG): two electrodes were positioned at theleft and right outer canthi (horizontal EOG) and two were placedaboveandbelowtherighteye.Additionally,electrocardiogramwasrecordedfromtwoelectrodesontheleftandrightforearm.FortheMEG measurement the head position within the MEG helmet hadto be assessed, thus positions of five index points and individualhead shapes were sampled using a digitizer.Datawerecorrectedforeyeandheartbeat-relatedartifactsusinga multiple source approach [1] implemented in BESA (MEGIS Soft- ware, Gräfeling, Germany). Afterwards the data were projectedfrom the 148 sensors onto a source montage consisting of eightregional sources analogously to our previous work [34]. A source modelwasgeneratedusingso-calledregionalsourcesconsistingof two orthogonal dipoles (the radial source is discarded) in order tocapture global activity independent of the orientation. Two of theeightsourceswereplacedsymmetricallyandbilaterallyintheaudi- Fig.1.  Correlationbetweentemporalalphaandgammapoweraveragedacrossbothtemporal sources. Black dots indicate values of tinnitus subjects; grey dots displayvalues of controls. tory cortex, which was the region of interest. The other six sourcesweredistributedoverthecortex:leftandrightprefrontalcortex,leftand right parietal cortex, anterior cingulum, and occipital cortex.The locations of sources were predefined by the authors, how-ever, and should therefore not be confused with the more preciseactivity localizations drawn from functional neuroimaging studies.The strength of applying a source montage is that the activity of brain regions of interest (i.e. left and right auditory cortex) can becaptured with a considerably reduced contribution of other con-currently active brain regions. Hence, the other six sources actedas a kind of spatial filter, sharpening the activity from the regionsof interest. The location of sources was identical for all subjects(adaptedtotheradiusofthesingle-spherefittedtotheheadshapeof theindividual)andcoveredroughlythewholevolume(fordetailedinformation concerning source montages see [25]). The leadfield wascomputedfortheregionsofinterestanditspseudo-inversewasused for calculation of the source strength. Data were then down-sampledto450HzandexportedtoMatlab(TheMathWorks,Natick,MA) for further analysis. For data analysis the entire 5min lengthwere used, analogously to our previous work [32,33]. The power- spectra for each source was averaged across orientations to yielda global estimate of the energy at that specific brain region. Therewasnodifferenceintheglobalpowerbetweentinnitusandcontrolsubjects. Normalized power was computed to minimize varianceresulting from strong interindividual variability. Linear regressionswerecalculatedfortheleftandtherighthemispherebetweenalpha(8–12) and gamma (40–90Hz; excluding 49–51Hz) power. Addi-tionally, group membership was considered as a factor in order touncoverpotentialdifferencesinregressionslopes.Thesignificancelevel was set at 5%.A strong negative correlation between temporal alpha andgamma power existed for tinnitus subjects ( r  = − .70,  p <.0001) aswell as for controls ( r  = − .74,  p <.001). These results are averagedacross both temporal sources (Fig. 1). Results for each side, respec- tively, are for tinnitus subjects left temporally ( r  = − .72,  p <.0001),right temporally ( r  = − .63,  p <.001) and for control subjects lefttemporally ( r  = − .79,  p <.0001), right temporally ( r  = − .65,  p <.01).Furthermore, the steepness of the regression lines for tinnitusand control subjects was compared to examine differences in thealpha–gamma relationship between tinnitus and control subjects.A significantly steeper slope was revealed for the tinnitus sub- jects ( F  =4.48,  p <.05) averaged across both temporal sources (left  I. Lorenz et al. / Neuroscience Letters 453 (2009) 225–228  227 temporallyseparately: F  =4.22,  p =.05,righttemporallyseparately: F  =3.82,  p =.06).Inthepresentworkwedemonstratedtheexistenceofaninverserelationship between auditory gamma and alpha activity in rest-ing tinnitus as well as in control subjects using MEG. This findingis in line with a prediction derived from the SLIM model out-lined in the introduction. The steepness of the regression lineswas compared for both groups to examine differences betweentinnitus and control subjects regarding the alpha–gamma pat-tern. Tinnitus subjects demonstrated a significantly steeper slopeof the regression line compared to controls, putatively caused bythe fact that a greater number of tinnitus subjects concurrentlyexhibit low alpha and high gamma power (Fig. 1). However, Fig. 1 clearly depicts a strong overlap between tinnitus and control sub- jects and shows that – despite being statistically significant – thegroup difference in slope is quite small. Hence, the question ariseswhy some subjects experience tinnitus while others with a similaralpha–gamma pattern do not. Different explanations are conceiv-ableforthisphenomenonandwouldrequirefurtherinvestigation:(1) alpha does not solely reflect the impact of an ongoing inhi-bition, but a complex mixture of several activities. Viewed froma macroscopic level it would not be possible to discern the var-ious mechanisms for resting data. (2) As suggested by SLIM, thecombination of enhanced slow-waves (most likely due to deaf-ferentation)combinedwithareductionofalpha-power(suggestedto be inhibitory) leads to enhanced gamma synchronization. Sincethere is no increase of slow-wave power in the healthy controlsubjects, a reduction of alpha does not lead to an increase ingamma. (3) A continuously enhanced level of synchronized activ-ity (via reduced inhibition) within the auditory cortex enhancesthebaselinesensitivityforneuronstosynchronizevianeuroplasticprocesses (e.g. enhanced synaptic strength), leading to a stabiliza-tion of the tinnitus-perception related activity. (4) The degree of synchronization/inhibitionwithintheauditorycortexisinfluencedby the dynamics in a widespread neuronal network exceeding theauditory cortex. Thus, whether one is experiencing a consciouspercept such as tinnitus depends strongly on how auditory cor-tical regions are likely to affect downstream higher-order brainregions. This could be achieved, e.g. by a higher output of audi-tory cortical regions (e.g. reflected in gamma activity) and/or ahighersensitivityofdownstreambrainregionstoprocesstheinputfrom auditory regions. In order to examine this issue further, stud-ies investigating the connectivity pattern between brain regions intinnitus as compared to controls will be highly informative. Someevidence for this explanation has recently been found in a studybyourgroupwhichrevealedafunctionalcorticalarchitecturewithaltered inter-areal synchronization in the alpha and gamma fre-quencies in tinnitus subjects [26]. Low inter-areal synchronization in the alpha network – as in the case of tinnitus – is accompa-nied by high synchronization in the gamma network. (5) A furtherphenomenonpotentiallyinfluencingthecurrentresults,whichhasbeen unaccounted for, are the individual differences between tin-nitussubjects.Thesesubjectsmaydifferaccordingtotheirhearingloss, their tinnitus duration or the quality of their tinnitus (puretoneorwhitenoisetinnitus)justtonameafew.Toourknowledge,there is no work correlating these factors to abnormal neuronaloscillations. There is, however, evidence from different TMS ther-apy studies that the amount of hearing loss, the tinnitus durationand the quality of the tinnitus seem to play an important role forthe treatment outcome [13,4]. (6) Our data only reflect a ‘snap- shot’ of cortical activity within a single subject. Therefore, not onlythe interindividual, but also the intraindividual variability comesinto play. A steeper slope in the alpha–gamma relationship couldindicateanalteredgainwithintinnitussufferers,whichisalsosug-gested by evoked auditory data [35,5]. As the level of inhibitory drive is downregulated in tinnitus, neurons in the auditory cortexsynchronize in a disproportionate manner. Thus, applied to spon-taneous data, repeated measurements within one subject wouldneed to be carefully investigated.Overall, despite confirming the notion that alpha is crucial inregulatingcorticalexcitabilityaswellasthesynchronizationwithincellassemblies,ourresultsindicatethatadysfunctionofthemech-anism underlying alpha could be a necessary but not a sufficientprerequisite for the development of tinnitus.A further question regarding our outcome is that the effect isclearly more pronounced within the left temporal source, whereasin the right temporal source only a trend could be revealed. Theseresults may be traced back to lateralization effects of the tinnitus.Nevertheless, this topic certainly requires further research.We did not find a linear correlation between changes in oscil-latory power and tinnitus symptoms (distress measured with theTinnitus Questionnaire [7]). It should be noted, however, that the subjective distress level in tinnitus is not correlated to psychoa-coustic measures [11,20,30]. Hence, we consider alpha reductions andgammaenhancementsinauditorybrainregionsnottobeinflu-enced by the distress level related to the tinnitus. Nevertheless, itwould be interesting in future to employ adequate psychoacousticmeasures of tinnitus in order to investigate whether the abnormaloscillatory patterns are related to basic psychoacoustical featuresof the tinnitus sensation.Another aspect to be taken into consideration regarding loweralpha power in tinnitus subjects is that these subjects may havehad a higher general arousal during the measurement due totheir knowledge that potential causes of their discomforting earnoise will be examined. This may have resulted in lower alphapower. However, we consider it to be highly unlikely that this hascaused a significant group effect regarding the slopes of the alphaandgammarelationship.Furthermore,wehaveexamined auditory alpha and gamma power, whereas arousal/relaxation would ratherbereflectedindecreased/enhanced  posterior  alphapower[29].Fur- thermore, the fact that the overall distress level is not related toalphaorgammapowerisanindicatorfortheeffectsnottoberesult-ingfromarousaldifferences(assumingthatdistressedparticipantsshould be more aroused).Within our framework, which was delineated in the introduc-tion (SLIM) [31], our current findings support the notion that reduced ongoing inhibition is associated with enhanced gammasynchronization in tinnitus and in control subjects. Our resultsare in line with previous research conducted by our group whichdemonstrated aberrant patterns of spontaneous neuronal activityintinnitussubjects,namelyreducedalphaandenhanceddeltaandgammapower[32].Sincealphahasbeendescribedasaninhibitory mechanism for the synchronization of power in higher frequen-cies [15,24,23], the strong reduction of alpha power in tinnitus subjects probably increases the likelihood of ‘spontaneous syn-chronization,macroscopicallyreflectedinincreasedgammapower.As mentioned above, however, this local type of synchronizationis not sufficient to fully explain the conscious perception of thetinnitus sound because it will also have to be taken into accountto what extent these processes affect downstream (higher-order)brain regions. This is an important issue when further developingthe SLIM model.In conclusion, the present MEG study provides support for aninverse relationship between auditory alpha and gamma bandactivity in resting spontaneous neuronal activity. This findingprovidesdirectsupportforourmodel(SLIM)inasmuchasaninter-ruptionoftheinhibitoryfunctionofthealpharhythmisassociatedwith synchronization in the gamma frequency range. With thesenovel findings regarding the strong negative association betweengamma and alpha band activity in general, further – more targeted–investigations(e.g.,inanimals)concerningthealpha–gammapat-tern in tinnitus would be important.  228  I. Lorenz et al. / Neuroscience Letters 453 (2009) 225–228  Acknowledgements This research was supported by the Deutsche Forschungsge-meinschaft (DFG) and the Tinnitus Research Initiative (TRI). Theauthors would like to thank Simona Müller for help during dataacquisition and Christian Lorenz for helpful comments on a draftof this article. 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