Functional reorganization of sensory processing following long-term neural adaptation to optical defects

Abstract

How we see is fundamentally limited by the eye's optics, which determine retinal image quality and constrain neural processing. Elucidating how long-term exposure to optical defects alters visual processing is vital for understanding the human brain's capacity for and limits of sensory plasticity. Using adaptive optics to bypass the eye's optical aberrations, we assessed changes in visual processing in neurotypically-developed adults with keratoconus (KC)-a corneal disease causing severe optical aberrations during adulthood that cannot be fully corrected using conventional methods. As a result, KC patients are chronically exposed to degraded retinal images in their everyday life, making them an ideal model to understand how prolonged exposure to poor optical quality alters visual processing. Here, we show that when tested under similar fully-corrected optical conditions as neurotypical observers, KC patients exhibited altered contrast sensitivity, with impaired sensitivity for fine spatial details and better sensitivity for coarse spatial details. Both gains and losses in contrast sensitivity were more pronounced in patients with poorer habitual optical quality. Moreover, using an equivalent noise paradigm and a computational model of visual processing, we show that these alterations in visual processing are mediated by changes in signal enhancement of spatial frequency selective mechanisms. The present findings uncover fundamental properties of neural compensation mechanisms in response to long-term exposure to optical defects, which alter sensory processing and limit the benefits of improved optics. The outcome is a large-scale functional reorganization favoring the processing of sensory information less affected by the eye's optics.Significance statement: The eye's optics represent an intrinsic limit to human visual perception, determining the quality of retinal images. Neural adaptation optimizes the brain's limited sensory processing capacity to the structure of the degraded retinal inputs, providing an exceptional quality of vision given these optical limitations. Here, we show that prolonged exposure to poor optical quality results in a functional reorganization of visual processing that favors sensory information less affected by the eye's optics. The present study helps elucidate how optical factors shape the way the brain processes visual information. Notably, the resulting adaptive neural plasticity limits the immediate perceptual benefits of optical interventions, a factor that must be taken into consideration when treating the increasing human population affected by optical defects.Understanding how we see requires insights into the contribution of both optical and neural factors mediating visual perception, from the processing of images formed on the retina to the resulting perceptual representations. Visual processing is fundamentally limited by the eye's optics, which determine retinal image quality and constrain performance. Human optics, however, are not fixed and can substantially change over o...

Asymmetries in visual acuity around the visual field

“…Starting at the level of the human eye, optical quality is not uniform across the retina (e.g., Curcio, Sloan, Kalina, & Hendrickson, 1990 ; Jaeken & Artal, 2012 ; Polans, Jaeken, McNabb, Artal, & Izatt, 2015 ; Song, Chui, Zhong, Elsner, & Burns, 2011 ; Thibos, Still, & Bradley, 1996 ; Zheleznyak, Barbot, Ghosh, & Yoon, 2016 ). Optical factors degrade retinal image quality, which can result in neural insensitivity to high-SF information (e.g., Barbot et al., 2020 ; Sabesan, Barbot, & Yoon, 2017 ; Sabesan & Yoon, 2009 ; Sawides, de Gracia, Dorronsoro, Webster, & Marcos, 2011 ). Both defocus and higher-order aberrations increase with eccentricity, with some differences as a function of polar angle ( Atchison & Scott, 2002 ; Lundström, Mira-Agudelo, & Artal, 2009 ).…”

Asymmetries in visual acuity around the visual field

“…Starting at the level of the human eye, optical quality is not uniform across the retina (e.g., Jaeken & Artal, 2012;Polans et al, 2015;Song et al, 2011;Zheleznyak et al, 2016). Optical factors chronically degrade retinal image quality, which can result in neural insensitivity to high-SF information (e.g., Barbot et al, 2020;Sabesan & Yoon, 2009;Sawides et al, 2011). Both defocus and higher-order aberrations increase with eccentricity, with some differences as a function of polar angle.…”

Optics and neural adaptation jointly limit human stereovision

“…It is plausible that this improvement in both contrast and phase congruency in a broadband stimulus, like the random-dot stereogram, allows the visual system to detect even smaller disparities than those resolved with well-focused normal optics. Further investigation is required to learn whether the binocular system can compensate for the phase disruption through long-term adaptation to the eyes' native optics and, if so, the extent to which the improvement in human stereopsis with perfect optics is compromised by phase adaptation (60,61).…”