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Auditory-Based Rehabilitation in the Visually Deprived Brain of Optic Auditory-based rehabilitation in the visually deprived brain of optic neuropathy patients Carina Sabourin Abstract Due to the extent humans rely on vision, sight restoration approaches are the predominant treatment option con- sidered for optic neuropathy patients with vision loss. This trend is refected in the wealth of research on sight restoration procedures. Patients with irreversible vision loss are left with limited treatment options due to the lack of research on alternative therapeutics and the prevalence of misdiagnosis (Jay 2016; Weerasinghe & Lueck 2016). Compensatory plasticity holds that auditory input can colonize the available cortical space in the visually deprived brain. The resulting enhancements in auditory cognition can be capitalized on by auditory-based rehabilitative tools. Sensory substitution devices have allowed visually deprived individuals to hear ‘colours’ and ‘shapes’, per- ceive their surroundings (Collignon, Champoux, Voss, & Lepore, 2011; Striem-Amit, Guendelman, & Amedi, 2012) and even read ‘written’ letters (Striem-Amit, Cohen, Dehaene, & Amedi, 2012) using soundscapes. VD echolocators navigate through daily obstacles using tongue clicks (Arnott, Thaler, Milne, Kish, & Goodale, 2013; A. J. Kolarik, Cirstea, Pardhan, & Moore, 2014; A. J. Kolarik, Scarfe, Moore, & Pardhan, 2017; Papadopoulos, Edwards, Row- an, & Allen, 2011; Teng, Puri, & Whitney, 2012; Teng & Whitney, 2011; Thaler, Arnott, & Goodale, 2011). Many higher order visual regions retain their functional specialization and adapt to auditory input from soundscapes or tongue clicks (O. Collignon, Lassonde, Lepore, Bastien, & Veraart, 2006; A. J. Kolarik et al. 2014; Striem-Amit & Amedi, 2014; Striem-Amit, Cohen, et al. 2012; Thaler et al. 2011). Due to the interaction between critical periods and plasticity, the therapeutic value of rehabilitative tools can vary with age of onset. Plasticity-induced cognitive enhancements from lack of visual stimulation during critical periods may underlie the greater efcacy of audi- tory-based rehabilitation for patients with early vision loss (Voss, 2019). Later vision loss improved the clinical outcome of sight restoration procedures. The addition of neuromodulators into other rehabilitative eforts may augment their therapeutic potential by promoting plasticity (Voss et al. 2016). While sight restoration may be the ideal rehabilitative procedure for optic neuropathy patients, auditory-based rehabilitative tools are valuable and underutilized treatment options when vision cannot be recovered. Introduction velopment (Behbehani, 2007). ON is classifed based on its Almost 300 million people worldwide are extensively visually mechanism before the exact aetiology can be determined (Bi- impaired, necessitating the need to develop efcacious reha- ousse & Newman, 2016) and appropriate clinical treatments bilitative tools from both a clinical and basic research per- can be considered. spective (WHO, 2012). Lack of one input will drive plasticity Correct diagnosis is often contingent on the accuracy of clin- to structurally and functionally change the brain to best com- ical examination and medical history (Biousse & Newman, pensate for the lost sense. Visual deprivation can be brought 2016). Several clinical characteristics are taken into consider- on by numerous pathologies and lead to enhancements in ation, such as visual deprivation onset, visual acuity, absence audition, particularly for individuals with optic neuropathy of the optic disc, nociceptive response to eye movements and (ON). ON refers to any damage to the optic nerve (CN II), colour vision (Biousse & Newman, 2016). Imaging may aid whether the insult was an isolated defect or the byproduct diagnosis, particularly in instances with infammation and of a greater neurological disorder. In instances of a great- infltration of the optic nerve (Becker et al. 2010; Davis & er disorder, ON is typically the initial clinical manifestation Newman, 1996; Jay, 2016). Magnetic resonance imaging of observed. ON often degenerates into optic atrophy. Optic both the brain and orbital may ascertain an underlying pa- atrophy, the loss of optic fbers, is the denouement of any thology, such as multiple sclerosis (MS) if a cerebral lesion is pathology in which neurons within the anterior visual sys- identifed (Balcer, Miller, Reingold, & Cohen, 2015). While tem are damaged. Despite the frequency of ON advancing to some argue electrophysiology is unnecessary (Jay, 2016), vi- optic atrophy, no clinical procedure, like neuroprotective or sually evoked responses may be used to identify ON to con- exogenic therapies, to restore sight exist (Behbehani, 2007). frm an uncertain MS or neuromyelitis diagnosis (Balcer et al. Translatable procedures like retinal ganglion cells and pho- 2015). Furthermore, when a diagnosis is difcult to ascertain, toreceptors replacement are stuck in the early stages of de- visually evoked response may be used to validate the presence 30 30 of ON (Jay, 2016; Odom et al. 2016). ONs and maculopathies pensatory changes can occur, due to the existence of criti- have similar clinical manifestations (Jay, 2016; Weerasing- cal periods. Critical periods, times in development when the he & Lueck, 2016) and may be confused during diagnosis. nervous system is especially vulnerable to change induced by Administration of the appropriate clinical management is a particular sensory input, vary the degree to which compen- contingent on the accurate diagnosis of the ON aetiology. satory plasticity can occur. For this reason, visually deprived A general diferential diagnosis can be made based on the individuals are classifed in this article according to onset of specifc characteristics of each potential diagnosis and the vision loss. Congenitally onset (CO) patients, those who are observed neuropathological defcits. The prevalence of ON visually deprived at birth and never experience visual input, misdiagnosis frequently impedes appropriate clinical man- are the most vulnerable to plasticity. Early onset (EO) and agement, sometimes to such an extent that sight restoration late onset (LO) individuals have a limited amount of visual treatments are no longer successful (Jay, 2016; Weerasinghe experience depending when vision loss occurs and adapt in & Lueck, 2016). The likelihood of sight recovery also varies a type-specifc manner. For individuals with ON for which with etiology, making efcient and correct diagnosis of the sight restoration treatments are inefective, rehabilitative ef- ON mechanism increasingly more essential. forts should capitalize on enhancements in the auditory cor- tex. While sight restoration is a viable option for many ON The complex etiology of optic neuropathy patients, those who are unlikely to recover their sight are The chance and extent of sight recovery seems to be large- often neglected in research on ON treatments. Furthermore, ly dependent on the exact etiology underlying the disorder. the impact of age of onset on ON clinical management is ON aetiologies are extremely heterogeneous, ranging from often unaccounted for. ON rehabilitative studies primarily exogenous factors like nutrient defciencies or trauma to the focus on sight restoration and neglect to investigate treatment optic nerve to endogenous defects, like hereditary mitochon- options for those of which sight restoration is not possible. drial diseases (Behbehani, 2007). About 35% of patents with The intent of this review is to describe critical periods within optic neuritis, a frequent manifestation of MS, fail to recover the context of the visual deprivation, the impact of critical vision and have scarce therapeutic options (Schinzel et al., periods on ON treatment as well as how rehabilitative eforts 2012). No efective treatment exists for Levber’s hereditary can capitalize on the cognitive diferences induced by com- ON, the most prevalent mitochondrial disease (Oostra, Bol- pensatory plasticity using auditory-based rehabilitative tools. huis, Wijburg, Zorn-Ende, & Bleeker-Wagemakers, 1994). Future research extending on the described fndings will also If identifed, ischemic ON can be categorized by the cause be suggested. As research on therapeutic options for ON pa- and location of blood fow loss (Miller, Newman, Biousse, & tients with irreversible vision loss is limited, studies on VD Kerrison, 2007). For example, anterior ischemic ON (AION) individuals with defects peripheral to optic chiasm will be refers to pathologies targeting the optic nerve head leading considered. to edema of the optic disc and rapidly progressing to monoc- ular vision deprivation (Foroozan, 2017). Medical treatments The impact of visual deprivation on critical periods and for AION fail to sufciently recover vision (Foroozan, 2017). considerations for rehabilitative eforts Similarly, iatrogenic ONs, like radiation ON, often lead to Age of vision loss is essential to consider in conjunction with extensive, irreversible vision loss subsequent to radiation cortical plasticity and critical ages, in which the brain is the therapies targeting lesions proximal to CN II (Thakkar et al. most adaptable. The input of a single sensory modality alone 2017). Few pathologies obscure the distinction between child- can greatly shape the development of brain structure and hood and adult varieties to the same extent as pediatric optic function. This was frst recognized to occur at a particular neuritis (PON) (Borchert, Liu, Pineles, & Waldman, 2017). period in development in a series of studies investigating
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