Abstract
The groundbreaking work of Hubel and Wiesel in the 1960’s on ocular dominance plasticity instigated many studies of the visual system of mammals, enriching our understanding of how the development of its structure and function depends on high quality visual input through both eyes. These studies have mainly employed lid suturing, dark rearing and eye patching applied to different species to reduce or impair visual input, and have created extensive knowledge on binocular vision. However, not all aspects and types of plasticity in the visual cortex have been covered in full detail. In that regard, a more drastic deprivation method like enucleation, leading to complete vision loss appears useful as it has more widespread effects on the afferent visual pathway and even on non-visual brain regions. One-eyed vision due to monocular enucleation (ME) profoundly affects the contralateral retinorecipient subcortical and cortical structures thereby creating a powerful means to investigate cortical plasticity phenomena in which binocular competition has no vote.In this review, we will present current knowledge about the specific application of ME as an experimental tool to study visual and cross-modal brain plasticity and compare early postnatal stages up into adulthood. The structural and physiological consequences of this type of extensive sensory loss as documented and studied in several animal species and human patients will be discussed. We will summarize how ME studies have been instrumental to our current understanding of the differentiation of sensory systems and how the structure and function of cortical circuits in mammals are shaped in response to such an extensive alteration in experience. In conclusion, we will highlight future perspectives and the clinical relevance of adding ME to the list of more longstanding deprivation models in visual system research.
Highlights
The capacity of the mammalian brain to rewire and physiologically modify neural connections in response to environmental changes is an intriguing and evolutionary conserved feature
Monocular enucleation-induced vision loss plasticity, are present across distributed neural networks in both juveniles and adults. They typically operate in parallel to allow specific changes at the molecular, cellular, systems and behavioral level as well as to allow compensational or homeostatic changes at the network level (Turrigiano and Nelson, 2000; Citri and Malenka, 2008; Holtmaat and Svoboda, 2009)
Accumulating evidence supports the presence of such plasticity in adulthood and even after partial sensory deprivation (Newton et al, 2002; Allman et al, 2009a; Meredith et al, 2012; Maslin et al, 2013) substantiating the notion of the capacity for brain plasticity throughout life
Summary
The capacity of the mammalian brain to rewire and physiologically modify neural connections in response to environmental changes is an intriguing and evolutionary conserved feature. A vast body of literature has demonstrated that the mature neocortex is not a fixed entity but retains substantial malleability, which is exemplified in primates (Kaas et al, 1983; Kaas, 1991; Donoghue, 1995; Gilbert, 1998; Qi et al, 2014), cat (Chino et al, 1995; Darian-Smith and Gilbert, 1995; Hu et al, 2009, 2010, 2011), ferret (Erisir and Harris, 2003; Allman et al, 2009a), raccoon (He et al, 2004), rat (Siucinska and Kossut, 1994; Kossut, 1998; Zhou et al, 2011; Tandon et al, 2013) and mouse (Keck et al, 2008; Lehmann and Löwel, 2008; MayaVetencourt et al, 2008; Van Brussel et al, 2011) In this context ME applied later in life has been a valuable research model since it could reveal additional plasticity and physiological modifications in the mature sensory cortex as compared to the other invasive and non-invasive vision impairment models (Newton et al, 2002; Paulussen et al, 2011b; Van Brussel et al, 2011; Nys et al, 2014). Similar to cytochrome oxidase activity patterns, Zif268 and c-Fos immunoreactivity after monocular deprivation (lid suture, enucleation and TTX injections) revealed ocular dominance columns as well as their respective size and density (Chaudhuri et al, 1995, 1997; Van der Gucht et al, 2000)
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