Macaque Area V2/V3 Reorganization Following Homonymous Retinal Lesions.

Georgios A Keliris,Michael C Schmid,Yibin Shao,Nikos K Logothetis,Stelios M Smirnakis,Mark Augath

doi:10.3389/fnins.2022.757091

Abstract

In the adult visual system, topographic reorganization of the primary visual cortex (V1) after retinal lesions has been extensively investigated. In contrast, the plasticity of higher order extrastriate areas following retinal lesions is less well studied. Here, we used fMRI to study reorganization of visual areas V2/V3 following the induction of permanent, binocular, homonymous retinal lesions in 4 adult macaque monkeys. We found that the great majority of voxels that did not show visual modulation on the day of the lesion in the V2/V3 lesion projection zone (LPZ) demonstrated significant visual modulations 2 weeks later, and the mean modulation strength remained approximately stable thereafter for the duration of our observations (4–5 months). The distribution of eccentricities of visually modulated voxels inside the V2/V3 LPZ spanned a wider range post-lesion than pre-lesion, suggesting that neurons inside the LPZ reorganize by receiving input either from the foveal or the peripheral border of the LPZ, depending on proximity. Overall, we conclude that area V2/V3 of adult rhesus macaques displays a significant capacity for topographic reorganization following retinal lesions markedly exceeding the corresponding capacity of area V1.

Highlights

Understanding the detailed capacity of the adult visual system for plasticity is important as it may inform the design of rehabilitative treatments aiming to enhance visual recovery after injury.Complete homonymous retinal injury eliminates the sensory input to retinotopically corresponding regions of visual cortex
In order to determine a stable and appropriate lesion projection zone (LPZ) for our V2/V3 analysis, we used the LPZ retinotopic coordinates carefully identified in V1 to guide our identification of the V2/V3 LPZ, instead of attempting to define the V2/V3 LPZ based on activity levels in the region which are expected to be variable over time
To be able to estimate the extent of this activity we have used the stimuli that included an artificial scotoma in the healthy hemisphere and evaluated the timecourse of activity within the V2/V3 artificial scotoma projection zone (ASPZ) defined in an identical way as the V2/V3 LPZ

Summary

Introduction

Complete homonymous retinal injury eliminates the sensory input to retinotopically corresponding regions of visual cortex. Since the 1990s several studies have focused on the reorganization of the primary visual cortex (V1) after homonymous retinal lesions, producing in part conflicting results. Several studies reported substantial reorganization in the primary visual cortex of cats and monkeys following retinal lesions (Kaas et al, 1990; Heinen and Skavenski, 1991; Gilbert and Wiesel, 1992; Calford et al, 2000; Giannikopoulos, 2006; Gilbert and Li, 2012). Found minimal, if any, topographic changes (Murakami et al, 1997; Horton and Hocking, 1998; Smirnakis et al, 2005). In a recent review, Wandell and Smirnakis (2009)

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