Perspective of functional magnetic resonance imaging in middle ear research

Abstract

Functional magnetic resonance imaging (MRI) studies have frequently been applied to study sensory system such as vision, language, and cognition, but have proceeded at a considerably slower speed in investigating middle ear and central auditory processing. This is due to several factors, including the intrinsic anatomy of the middle ear system and inherent acoustic noise during acquisition of MRI data. However, accumulating evidences have demonstrated that clarification of some fundamental neural underpinnings of audition associated with middle ear mechanics can be achieved using functional MRI methods. This mini review attempted to take a narrow snapshot of the currently available functional MRI procedures and gave examples of what may be learned about hearing from their application. It is hoped that with these technical advancements, many new high impact applications in audition would follow. In particular, because the fMRI can be used in humans and in animals, fMRI may represent a unique tool that should promote translational research by enabling parallel analyses of physiological and pathological processes in the human and animal auditory system.

This article is part of a Special Issue entitled “MEMRO 2012”.

Introduction

Mechanically, sound is the vibration of air and is transmitted as a vibration through the tympanic membrane, via the auditory ossicles to the oval window. Mechanical conduction of sound is then converted to electrochemical impulses in the organ of Corti of the cochlea, which acts as a neural transducer (Farris et al., 2006; Kitajiri et al., 2010). Sound evoked neuronal activity then propagates through the auditory pathway, which is composed of the cochlea, cochlear nucleus, superior olivary complex, lateral lemniscus, inferior colliculus, and medial geniculate body, to the auditory cortex (Muller-Preuss and Mitzdorf, 1984; Nieuwenhuys, 1984). Therefore, changes in mechanical conduction of sound originating from the middle ear would affect neuronal activity in the central auditory system. For example, middle ear sensitivity, such as sound pressure variations on the tympanic membrane, resulted in pressure dependent cortical representation (Job et al., 2011).

Functional magnetic resonance (MR) imaging technique, which is relatively new in middle ear research, has mainly been used to address two questions; (1) tonotopic organization of the central auditory pathway in response to frequency and intensity of sound stimuli and (2) auditory cortical mapping in response to other features of sound stimuli, such as complex stimuli. Regarding tonotopic organization, much of our current understanding of tonotopic organization has been attained primarily through use of invasive techniques, such as electrophysiology (Merzenich et al., 1975; Recanzone et al., 2000; Malmierca et al., 2008), immunohistochemical assay (Ehret and Fischer, 1991; Pierson and Snyder-Keller, 1994), and 2-deoxyglucose labeling (Huang and Fex, 1986). However, electrophysiological recordings cannot achieve the continuous spatial coverage and large field of view (FOV) required for thorough study of tonotopic organization. Immunohistochemical study would require use of a large number of animals in order to cover a broad frequency range and is difficult to use in longitudinal investigations. In contrast to these techniques, non-invasive functional MR imaging has a large field of view and can allow for simultaneous examination of multiple auditory structures (Jancke et al., 1998; Sigalovsky and Melcher, 2006). In auditory cortical mapping in response to complex stimuli, a number of studies using fMRI have examined the pitch representation in the auditory cortex. In addition, a recent connectivity study using fMRI challenged the traditional view that sound is processed almost exclusively in the auditory pathway unless sound is imbued with behavioral significance. Obviously, vocalization, musical experience, and stimuli with cognitive context are a type of complex sound stimuli. However, a detailed discussion of these issues is beyond the scope of this mini-review.

In this mini review, we focused on the possible applications of functional MR imaging for investigation of the relationship between sound stimuli (simple and complex stimuli) in the middle ear and its central neural processing. Among functional MR imaging techniques, neuro-functional MRI (fMRI) is a method used in brain mapping. In addition, manganese enhanced MRI (MEMRI) has recently been introduced as an important functional imaging tool for the study of neural signal conduction from the middle ear to the central auditory pathway with very high spatial resolution. We also discussed the intrinsic limitation of fMRI (acoustic MR scanner noise) and possible solutions. It is not the purpose of this paper to provide a complete description of the physics and mathematical algorithms associated with functional MR imaging. Other reports have addressed these issues in detail (references). However, it is appropriate to provide brief descriptions of the functional MR imaging techniques that, to date, have been applied to the study of hearing, or that offer potential for such applications. In addition, it is not the purpose of this report to provide a critical evaluation of the clinical applications of functional MR imaging. Clinical applications of functional MR imaging are still in their infancy.