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A Window Into Visual Cortex Development and Recovery of Vision: Introduction to the Vision Research Special Issue on Amblyopia

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A Window Into Visual Cortex Development and Recovery of Vision: Introduction to the Vision Research Special Issue on Amblyopia Vision Research 114 (2015) 1–3 Contents lists available at ScienceDirect Vision Research journal homepage: www.elsevier.com/locate/visres Preface A window into visual cortex development and recovery of vision: Introduction to the Vision Research special issue on Amblyopia Normal visual development requires unimpeded and coordi- developmental ages on the structure and function of primary nated input from each eye to the visual cortex during an early crit- visual cortex (Hubel & Weisel, 2004). More recently, work in this ical period of cortical maturation. Disrupted binocular vision area has provided new insights into the impact of abnormal visual during this critical period, due to visual deprivation (e.g. congenital experience on the development of extrastriate visual brain areas cataract), misalignment of the eyes (strabismus) or unequal refrac- (Bi et al., 2011; El-Shamayleh et al., 2010) and provided unex- tive error (anisometropia), can lead to amblyopia, a neurodevelop- pected evidence that vision can indeed be recovered in the ambly- mental disorder of vision (Daw, 2014; Holmes & Clarke, 2006). opic eyes of visually mature animals (Duffy & Mitchell, 2013; Amblyopia is characterized by a loss of visual acuity in the affected Murphy et al., 2015). This suggests that critical periods are not eye and impaired or absent binocular visual function in the absolute. Recovery of vision has also been demonstrated in adult absence of any ocular disease or abnormality. humans with amblyopia, further supporting this idea (Astle, Amblyopia has been the focus of two parallel and complemen- Webb, & McGraw, 2011; Hess, Thompson, & Baker, 2014; Levi & tary lines of research for many decades: one clinical and one neu- Li, 2009). roscientific. Clinically, amblyopia represents the most common The breadth and momentum of amblyopia research was cause of visual impairment in childhood (Wong, 2012) and has a recently recognized by joint mini-symposia organized by the Eye significant impact on quality of life (Carlton & Kaltenthaler, Movements/Strabismus/Amblyopia/Neuro-ophthalmology (EY) 2011). The current evidence-based treatment for amblyopia and Visual Psychophysics/Physiological Optics (VI) sections of the involves refractive correction (Cotter et al., 2006; Writing Association for Research in Vision and Ophthalmology (ARVO), Committee for the Pediatric Eye Disease Investigator et al., 2012) held at the 2014 ARVO annual meeting. The symposia brought followed by occlusion or penalization of the non-amblyopic eye together researchers whose combined expertise spanned both to encourage use of the amblyopic eye (Pediatric Eye Disease the clinical and neuroscientific areas of amblyopia research and Investigator Group, 2002). This treatment can induce recovery of provided the inspiration for this special issue. amblyopic eye visual acuity if implemented at an early age The special issue highlights a number of key themes in ambly- (Wallace et al., 2006); however improvements in binocular vision opia research that bring together these two important lines of are often limited (Birch, 2013). research. The first relates to the nature of the structural and func- In humans, early monocular deprivation has catastrophic conse- tional abnormalities that underlie the visual deficits caused by quences for the final level of vision the deprived eye can obtain, amblyopia. With regards to cortical structure, Allen et al. (2015) while the same type of deprivation introduced later in childhood used diffusion tensor imaging to identify and assess white matter has a diminishing impact and little or no effect at all beyond tracts within the visual pathways in a group of adult patients with around 9 years of age (Vaegan & Taylor, 1979). This transition from amblyopia and a group of controls. Patients with amblyopia exhib- severe early impairments to virtually no effect on acuity later in ited increased mean diffusivity in thalamo-cortical visual path- development delimits the duration of visual system susceptibility ways, but no significant differences between patients and to abnormal visual experience – the so-called ‘critical period’. controls were observed in cortico-cortical pathways. This suggests This window is thought to reflect a changing balance of influence that amblyopia may alter the white matter properties of early between visual mechanisms of plasticity and stability. Currently, visual pathways. there are no treatments for adults with amblyopia that are in gen- A number of advances in understanding the neural changes that eral clinical use. This reflects the rather entrenched view that occur in amblyopia are also reported in the special issue. Using amblyopia is intractable in older patients. Once the period of vul- multi-electrode recordings from V1 and V2 in macaques with nerability had passed, it was assumed that plasticity was limited experimentally induced amblyopia, Shooner et al. (2015) demon- in scope and, as a result, treatment would be ineffective. strated that more information from the amblyopic eye is available From a neuroscientific perspective, amblyopia is a preeminent at an early stage of cortical processing than would be expected model for exploring cortical development and plasticity in both based on behavioral contrast sensitivity losses. This implies deficits animals and humans. Nobel prize winners Hubel and Wiesel in downstream processing. Shooner et al. (2015) identified a reduc- famously used experimentally induced amblyopia in monkeys to tion in the relative proportion of signals passing to extrastriate investigate the impact of altered visual input at different areas due to sub-optimal pooling of neural information from the http://dx.doi.org/10.1016/j.visres.2015.06.002 0042-6989/Ó 2015 Elsevier Ltd. All rights reserved. 2 Preface / Vision Research 114 (2015) 1–3 amblyopic eye within V1 and V2 as a potential mechanism for this novel hypothesis that interocular suppression could be used to dif- effect. In a neurobiological study, Williams et al. (2015) investi- ferentiate amblyopia from myopia in the context of vision screen- gated the changes that occur within V1 in a cat model of monocu- ing. They found that a measure of interocular inhibition was highly lar deprivation amblyopia and found a rapid loss of AMPA receptor accurate in discriminating amblyopic eyes from myopic eyes with proteins across all of V1, that was followed by a more gradual or without the presence of refractive correction. With respect to recovery in peripheral visual field representations. The net result the treatment of amblyopia, Kelly et al. (2015) used visually was a loss of AMPA receptors that persisted only in the central evoked potentials (VEPs) to investigate the effect of occlusion ther- region of V1. Importantly, Williams et al. (2015) propose a link apy on the cortical response to information from the amblyopic between the deprivation-induced loss of AMPA receptors in V1 eye. Prior to treatment, amblyopic eye VEPs exhibited a poorer sig- and visual acuity impairments in the central field that were appar- nal-to-noise ratio, a longer latency and increased phase misalign- ent even under binocular viewing conditions in monocularly ment relative to fellow eye VEPs. Each of these measures deprived animals. Also using a cat model of amblyopia, Crewther improved with occlusion therapy, revealing a change in visual cor- and Crewther (2015) report neurophysiological and modeling evi- tex function that was partially related to improved temporal syn- dence indicating that differences in the timing of signals from each chronization of neural activity. eye propagating from LGN to V1 play a role in the loss of visual The final three research papers within the detection and treat- function associated with strabismic amblyopia. In particular, an ment theme all involve binocular treatment of amblyopia. Duffy increased temporal dispersion of signals from the amblyopic eye et al. (2015) build on their earlier finding that exposure to com- relative to the fellow eye was evident in single cell extracellular plete darkness enabled recovery of vision in kittens with monocu- recordings made from the LGN. lar deprivation amblyopia (Duffy & Mitchell, 2013) by asking The second theme relates to the impact of amblyopia on visual whether binocular eyelid closure initiates the same effect. functions over and above the loss of visual acuity in the amblyopic Although binocular eyelid closure led to anatomical recovery of eye. Using retinal imaging, Chung et al. (2015) investigated the neuron soma size in deprived layers of the LGN, no behavioral effect of strabismic and anisometropic amblyopia on fixational improvements occurred. Subsequent exposure to complete dark- eye movements. While fixational eye movements in the non-am- ness led to recovery of vision in the deprived eye, suggesting that blyopic eyes of patients were not different from controls, ambly- a complete absence of binocular visual input is required for the opic eyes exhibited abnormal fixational eye movements, an effect behavioral therapeutic effect. Using an active intervention strategy that was particularly pronounced in patients with strabismic in human patients, Li et al. (2015) report significant improvements amblyopia. Further, Chung et al. (2015) highlighted the functional in amblyopic eye contrast sensitivity in adult patients following relevance of eye-movement anomalies in amblyopia by identifying treatment with a dichoptic video game based therapy developed the characteristics of fixational eye movements that limit
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