Melbourne School of Psychological Sciences - Theses
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ItemThe neuroprotective effects of music training in epilepsy( 2018)Music is central to modern life and ubiquitous in human culture. A unique functional neurobiological property of music is its greater bilateral representation in the brain, which is hypothesised to account for the proposed relative preservation of music functions in the face of neurological injury, particularly the paroxysmal ictal and inter-ictal network disruption associated with focal epilepsy. Furthermore, specialised training in music may enhance this ‘neuroresilience’ of music functions, in addition to potentially protecting the brain against the effects of future neurological disruption on non-music cognitive abilities. The neurobiological mechanisms underpinning music-related neuroresilience and neuroprotection, however, remain unclear. The current thesis therefore explored these two themes of cognitive resilience and the potential neuroprotective effects of music training, through the critical analysis of extant literature describing music and non-music cognitive abilities in non-musicians (Chapter 2) and musicians (Chapter 4) with neurological disorders, a case-control experimental group study investigating music-related resilience and neuroprotection using the neurological model of focal epilepsy (Chapter 3), and a case study describing the unique preservation of music (but not verbal) memory in a musician with bilateral temporal lobe epilepsy (Chapter 5). Chapter 2 comprehensively reviewed 65 studies examining a range of music functions in pre-surgical or post-surgical non-musicians with focal epilepsy. Overall, the findings of this review provided evidence that music cognitive deficits are relatively common in non-musicians with epilepsy, with many domains affected in at least half of the patient cohorts. Considerable variability in impairment was evident, however, with post-surgical epilepsy cohorts tending to exhibit more frequent deficits than pre-surgical patients. This was especially evident for music functions associated with broader, multi-domain networks (e.g., melodic and musical emotion processing) compared to lower-level musical processing (e.g., pitch discrimination). A rightward asymmetry was observed for many music deficits, particularly for the domains of melodic processing and singing. Although these results contradicted the idea of music’s resistance to disease and the benefits of bilateral functional organisation, a number of limitations were identified within this literature, which made the interpretation of the findings challenging. Critically, examination of music cognitive abilities in isolation from non-music functions such as language and verbal memory does not allow for the comparison of the relative neuroresilience of music versus non-music skills. Consequently, the case-control group study presented in Chapter 3 assessed music and non-music cognition in focal epilepsy patients with and without music training, and healthy control participants with and without music training. The results indicated a pervasive pattern of verbal cognitive impairments (e.g., verbal fluency, abstract reasoning, and memory) and select music cognitive difficulties (melodic discrimination and metre identification) in epilepsy non-musicians compared to controls (musicians and non-musicians combined). In contrast, epilepsy musicians displayed preserved verbal cognition on all measures except verbal fluency, and no significant deficits in music cognition. The results were interpreted as a neuroprotective effect of music training in the epilepsy musician group, which benefited cognitive abilities that likely share processing components and neural substrates with the skills required to learn to play an instrument. This includes training-related enhancement of brain regions in fronto-temporo-parietal networks and their underlying structural connections (e.g., superior longitudinal and arcuate fasciculi), which support core cognitive processes such as working memory and executive control. This interpretation was strengthened by the finding that musicians who began training earlier in life (<=7 years old) tended to display greater benefits for verbal cognitive abilities. Furthermore, the overall more pervasive pattern of non-music cognitive deficits in patient non-musicians supported the notion of music’s greater relative resilience to the cognitive consequences of epilepsy. The critical literature review in Chapter 4 extended the findings of Chapter 3, by synthesising the evidence from 87 studies (comprising 99 unique cases) of musicians with either epilepsy, stroke, dementia, herpes simplex virus encephalitis, and patients undergoing surgical resection of brain tumours. The collated findings across populations indicated that impairment was generally more commonly reported for non-music compared to music cognitive functions, and that the frequency of music and non-music impairments varied as a function of disease aetiology. A comparison between epilepsy, stroke, and dementia cases revealed the greatest levels of music and non-music functional preservation in epilepsy musicians. Moreover, epilepsy musicians demonstrated fewer overall deficits in music versus non-music domains, with only select impairments in language, verbal/visual memory, attention, and music reading. These findings reinforced the results from Chapter 3, highlighting the relative neuroresilience of music functions, and the protective effects of music training in epilepsy. Given the more widespread patterns of impairment observed in stroke and dementia cases, however, music training does not appear to provide neuroprotection for untrained abilities (i.e., ‘far’ transfer) in patients with sudden acute neurological insult (stroke) or diffuse and progressive cerebral atrophy (dementia). Finally, Chapter 5 described the case of a particularly interesting musician with bilateral temporal lobe epilepsy and hippocampal sclerosis, who had taken part in the group study from Chapter 3. This musician (BK) exhibited a profound discrepancy between his intact melodic learning and memory skills and severely impaired verbal and visual memory, illustrating the possible upper limits to the potential for music training to compensate for bilateral temporal lobe disruption. BK’s preserved music memory was intriguing, and it was hypothsised that he was engaging the dorsal fronto-temporal circuit implicated in working memory and articulatory rehearsal, to facilitate the encoding, storage, and retrieval of musical information. To investigate this further, BK was assessed on a task of melodic learning with articulatory suppression, involving trials of digit span forward serial recall after the presentation of each of eight short, novel melodic sequences that he was to remember. Comparison with his performance on the same task without phonological interference revealed a disruptive effect of the extraneous auditory information for remembering atonal melodic sequences. This suggested that articulatory rehearsal was an effective encoding strategy for processing and remembering these stimuli, implicating at least partial mediation of BK’s music memory via training-enhanced working memory circuits. These intriguing findings provided further evidence for the beneficial effects of music training-related neuroplasticity for multiple music and non-music cognitive systems, in addition to emphasising the relative resilience of music functions, against the effects of even severe bilateral network disruption. As suggested by Chapter 4, these benefits appear to be unique and specific to epilepsy, and do not provide the same level of cognitive sparing in musicians with non-epileptic bilateral neurological damage. This thesis discusses the above findings in the context of methodological limitations in the music neuroscience literature, including a dearth of group studies comparing musicians and non-musicians with neurological disorders. These findings have critical implications for music education, emphasising the importance of access to music within schools, in light of the evidence that engaging in music learning early in life may be associated with neuroplastic changes that benefit the brain and cognition later in life. In addition, examination of the possible therapeutic effects of music training in individuals with epilepsy may shed further light on the neurobiological mechanisms underpinning music-related neuroplasticity, and how time-sensitive these processes are in relation to the development of seizures.