Functional and metabolic brain correlates in hearing loss and rehabilitation

Abstract

The human auditory system serves the role of extracting information from objects in the environment engaging in analyses of the auditory world so that the listener can accomplish the goal of learning and communication. Several shreds of evidence demonstrate that disorders of one part of the auditory system often affect the function of other parts of it. This is especially apparent with regard to hyperactive disorders, but even noise-induced and age-related hearing loss (ARHL) are not isolated cochlear phenomena, but the auditory nervous system, in its different stages, is involved in these pathologic states, and consequently it is no longer valid the sharp division of disorders into peripheral and central. ARHL is one of the most common chronic health conditions affecting older adults and its high prevalence compels different research fields from audiologists, otolaryngologists, to neuroscientists, dedicated to understand the different mechanisms underlying this disorder and so that effective prevention, intervention, and rehabilitative strategies can be developed to ameliorate the quality of life of people affected. Historically, the impetus for investigations of ARHL was Professor Schuknecht’s description in 1974, whose observations have underscored that ARHL is a complex phenomenon manifested in different forms among individuals. Today investigators recognize that hearing ability in advancing age results from a combination of different factors and that there is an association with cognitive-related process disruption and brain alteration, hypothesizing the presence of a link between ARHL, cognitive impairment, and dementia. The sole possible rehabilitation process, in case of hearing deficit, is the use of a hearing aid, a device whose only charge is the amplification of the auditory input into the ear canal, but whose daily and prolonged usage and its interaction and effects on the multifactorial nature of the pathology are still unclear. In this context, the aim of the research project reported in this thesis is the investigation about ARHL signs on the central nervous system, with additional attention to the effects of auditory rehabilitation with prolonged and continuous hearing aids usage during normal daily life. In order to address these issues, magnetic resonance imaging (MRI) was used to study the human brain in vivo and non-invasively, since it was already widely applied for the study of neurological and psychiatric disorders as well as to understand the basis of neural physiological processes and sensory perception. The first aim of this work is concentrated on the neural modification linked to ARHL in the primary auditory cortex, the entry point of the auditory signal in the central nervous system. For this purpose, in chapter 2 and chapter 3 the attention is dedicated to the analysis of the human primary auditory cortex in ARHL patients using innovative MRI methodologies to map the basal metabolic neuronal activity. Indeed, brain images of a group of ARHL patients and age- and sex-matched healthy normal hearing controls have been acquired to analyze the cerebral metabolic changes and to possible link those to the pathological course. A local cortical hypometabolic pattern is revealed in the right primary auditory cortex that was found to be related to the audiogram steepness, that is, the difference in hearing loss relative to adjacent frequencies. Therefore, these new pieces of information were used to classify the different types of presbycusis and their relationship to different local cortical metabolic patterns in auditory cortex consequently showing how a classification based on multiple audiological features can individuate groups of patients with different hypometabolic cortical pattern and possibly different pathological etiology. Then the second aim, presented in chapter 4 and chapter 5, is to expand the point of view from the local perspective to a more global view (on the entire brain) in a dual way: (i) combining the metabolic information with a whole brain functional connectivity analysis, to explore if and how the localized hypometabolic pattern in primary auditory cortex influences the global brain connectivity or drag a general reallocation of resources and a functional brain reorganization and (ii) using a longitudinal experimental framework, explore how all those brain changes interact when ARHL patients follow a rehabilitation period with continuous usage of hearing aids devices with an additional focus on the neuropsychological profile. In this case, the impact of HL condition (and its subsequent hearing aids mediated rehabilitation) was highlighted on the long-range neural communication between the primary auditory cortex and higher-order brain regions, suggesting that the hypoperfused early auditory cortex could be a seed place where different neuroplastic changes originate. Together with the functional and metabolic analysis, the neuropsychological evaluation underlies the presence of an executive and attentional impairment in HL population. Therefore, it was proved for the first time, that the prolonged use of hearing aid devices, is not able to reverse the reduced activity in the primary sensory cortex, but can cause a global functional reorganization especially concentrated in the communication between the primary sensory centers and multimodal key areas of the frontal and temporal lobes as well as an improvement in visuo-spatial abilities only in patients whose hearing deficit is limited. [edited by Author]