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Capturing Activity Along the Auditory Nerve

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Capturing Activity Along the Auditory Nerve Into the deep – Capturing activity along the auditory nerve Masterarbeit An der Naturwissenschaftlichen Fakultät der Paris-Lodron-Universität Salzburg im Sommersemester 2018 Eingereicht von Fabian Schmidt Matrikelnummer: 1222361 Gutachter Univ.-Prof. Dr. Nathan Weisz Fachbereich Psychologie INTO THE DEEP 2 Abstract Early auditory evoked potentials occur within the first ten milliseconds after acoustic stimulation. The recording of these potentials usually consists of five to seven vertex positive waves, with Wave I & II being related to activity in the auditory nerve and the cochlear nucleus. The most common used methods of measuring these electrical signals spreading through the auditory pathway are Electrocochleography (ECochG) and the Auditory Brainstem Response (ABR). As the recorded signals are typically weak in amplitude, averaging over a lot of trials, elicited by simple stimuli such as clicks or tone bursts, is required to obtain a reliable response. The large amount of repetitive trials presents a challenge to researchers trying to investigate auditory nerve activity during a more natural stimulation (e.g. listening to running speech). The present study shows, that by combining ECochG, ABR and magnetoencephalography (MEG) using a forward/backward encoding modelling approach, a “pipeline” to the auditory nerve can be built. Results suggest that activity presumably generated by the auditory nerve, can be captured in the MEG. Furthermore, it was shown that early auditory evoked potentials can be reconstructed and used to create a prediction model for the activity along the auditory pathway. This opens the gates to further investigate auditory nerve activity under more natural circumstances (e.g. listening to running speech). keywords: auditory nerve; auditory pathway; cochlear nucleus; early auditory evoked potentials; electrocochleography; magnetoencephalography; auditory brainstem response INTO THE DEEP 3 Zusammenfassung Frühe auditorische evozierte Potentiale ereignen sich in den ersten zehn Millisekunden nach einem akustischen Reiz. Das gemessene Signal besteht in der Regel aus fünf bis sieben Vertex positiven Wellen. Die ersten beiden Wellen (I/II) sind assoziiert mit Aktivität im Hörnerv und den Schneckenkernen. Die am häufigsten verwendeten Methoden zur Messung dieser elektrischen Signale, auf ihrem Weg durch das auditive System, sind Elektrocochleographie (EcochG) und die Hirnstammaudiometrie (BERA). Da die aufgezeichneten Signale typischerweise eine geringe Amplitude haben, ist eine Mittelwertbildung über viele „Trials“ (ausgelöst durch Klicks oder „tone bursts“) erforderlich, um ein deutliches Signal zu erkennen. Dies begrenzt die Fähigkeiten von Forschern, die versuchen, die Aktivität des Hörnervs unter einer natürlichen Stimulation (z. B. mit laufender Sprache) zu untersuchen. Die vorliegende Studie zeigt, dass durch Kombination von ECochG, BERA und Magnetoenzephalographie (MEG) mit einem Vorwärts/Rückwärts- codierungsmodells eine "Pipeline" zum Hörnerv aufgebaut werden kann. Die Ergebnisse dieser Studie deuten darauf hin, dass die Aktivität, die vermutlich vom Hörnerv generiert wird, im MEG erfasst werden kann. Darüber hinaus konnte gezeigt werden, dass frühe auditorisch evozierte Potentiale rekonstruiert und genutzt werden können, um ein Vorhersagemodell für die Aktivität entlang des Hörnervs zu erstellen. Dies öffnet die Tore, um die Aktivität des Hörnervs während einer natürlicheren Stimulation (z. B. mit laufender Sprache) weiter zu untersuchen. Stichworte: Hörnerv; auditives System; Schneckenkerne; frühe auditorisch evozierte Potentiale; Elektrocochleographie; Magnetenenzephalographie, Hirnstammaudiometrie INTO THE DEEP 4 Introduction After a sound hits the eardrum, within 10 milliseconds, a series of sub-cortical potentials can be measured. The recording of these early auditory evoked potentials usually consists of five to seven vertex positive waves, denoted in roman numerals ranging from I to VII (Jewett & Williston, 1971). These waves are typically analyzed by clinicians to provide diagnostic value in patients with hearing disorders. In practice, when measuring these potentials, clinicians are usually only able to orient themselves on differences in latency and amplitude of the individual peaks, generated by clicks or tone bursts (Eggermont, 2017; Ferraro, 2010). However, even among normal hearing subjects’ distinct peaks (especially for Wave II, IV and VI) remain sometimes undetectable (Levine et al., 1993). The absence of these peaks can be partially explained by the generally low amplitude of the early evoked potentials (Jewett & Williston, 1971; Zhang, McAllister, Scotney, McClean, & Houston, 2006). This makes it usually necessary to average over thousands of trials to extract the activity from the background electroencephalographic signal (Jewett & Williston, 1971; Zhang et al., 2006). In the last four decades a vast amount of research ranging from animal models (Melcher & Kiang, 1996) to direct measurements of the auditory nerve and selected brainstem areas (Hashimoto, Ishiyama, Yoshimoto, & Nemoto, 1981; Møller & Jannetta, 1985; Møller, Jho, Yokota & Jannetta, 1995; Rattay & Danner, 2014; Tait, Miller, Cycowicz & Sohmer, 1987) was conducted to identify the generators of the early evoked potentials. Human intracranial nearfield recordings provide convincing evidence, that Wave I and Wave II are generated by the auditory nerve (Møller et al., 1995) with a possible contribution from the cochlear nucleus for wave II (Hashimoto et al., 1981). Estimating the origins of Wave III and IV poses a bigger challenge. It is not yet clear whether Wave III is produced by the ipsilateral cochlear nucleus or the superior olivary complex and if Wave IV originates in the cochlear nucleus and/or in INTO THE DEEP 5 the nuclei of the superior olivary complex (Møller & Jannetta, 1985; Møller et al., 1995). Intracranial recordings show that Wave V, the most prominent wave detected in humans, is primarily attributed to activity in the lateral leminiscus and the inferior colliculi (Møller et al. 1995). For Wave VI & VII only, sparse evidence exists in terms of their generation sites, as they usually only appear in few subjects. According to Brugge et al. (2009) the earliest cortical responses to acoustic stimulation occur at 9-12ms. One could hypothesize that with a latency of 9-10ms Wave VII could thus be generated by the primary auditory cortex. Here it should be noted, that all investigators focused on the identification of the evoked responses in humans used invasive techniques, making them not applicable in most clinical settings (e.g. hearing screenings). Due to their distance to the sensors it has been disputable, if signals originating in deep sub- cortical structures such as the lateral leminiscus (Wave V) can be detected by using magnetoencephalography (MEG). So far, only Parkkonen, Fujiki & Mäkelä (2009) managed to estimate the source locations of Wave I, II, and V using MEG. This is attributed to the difficulties in recording and modeling these signals, without the use of advanced analysis techniques (Simpson & Prendergast, 2013). In their study, Parkonnen et al. (2009) used only surface-EEG electrodes as a reference signal to the activity measured by the MEG. Whilst getting a good resolution for responses related to late brainstem activity (Wave V), their design was not optimized for the measurement of the early evoked activity originating in the auditory nerve and the cochlear nucleus (Wave I & II). Electrocochleography (ECochG) is one of the most common used methods by audiologists to measure electrical activity produced in the cochlea after acoustic stimulation. ECochG enables the investigators to follow the electrical signals generated in the cochlea as they spread through the auditory pathway across the brainstem into the auditory cortex. Clinicians usually apply ECochG for the diagnosis of Ménière’s disease by investigating INTO THE DEEP 6 abnormalities of the summating potential (SP) and the compound action potential (CAP) (Eggermont, 2017). The CAP is corresponding to the first wave captured when measuring the early auditory evoked potentials (Minaya & Etcherson, 2015). In general, it can be differentiated between two major ways of measuring ECochG (extra-tympanic (ET) and trans-tympanic (TT) ECochG (Ferraro, 2010). Whilst ET-ECochG is non-invasively recorded from the external ear canal close to the tympanic membrane, TT-ECochG involves piercing a needle electrode through the tympanic membrane measuring the activity at the promontory close to the round window (Bonucci & Hyppolito, 2009). Both methods do not show different results regarding the latency of the measured peaks (Eggermont, 2017). However, due to the proximity of the electrode to the cochlea, the amplitudes of the signals are approximately four times larger in TT-ECochG compared to ET-ECochG (Ferraro & Durrant, 2006). As a downside, due to its invasive nature, TT-ECochG always involves a clinician to be present for electrode placements and subjects willing getting their tympanic membrane pierced, making it in general harder to implement in a non-clinical setting (Bonucci & Hyppolito, 2009). Another common method applied by audiologists for the measurements of early acoustic activity is the auditory brainstem response (ABR). The ABR is a far-field recording typically measured by placing a single electrode on the scalp at either FpZ or Cz (Crumley, 2011). As no special in-ear electrodes are needed to measure the ABR it is usually
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