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Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects
Authors:Amalia Papanikolaou  Georgios A. Keliris  T. Dorina Papageorgiou  Yibin Shao  Elke Krapp  Eleni Papageorgiou  Katarina Stingl  Anna Bruckmann  Ulrich Schiefer  Nikos K. Logothetis  Stelios M. Smirnakis
Abstract:Injury to the primary visual cortex (V1) typically leads to loss of conscious vision in the corresponding, homonymous region of the contralateral visual hemifield (scotoma). Several studies suggest that V1 is highly plastic after injury to the visual pathways, whereas others have called this conclusion into question. We used functional magnetic resonance imaging (fMRI) to measure area V1 population receptive field (pRF) properties in five patients with partial or complete quadrantic visual field loss as a result of partial V1+ or optic radiation lesions. Comparisons were made with healthy controls deprived of visual stimulation in one quadrant [“artificial scotoma” (AS)]. We observed no large-scale changes in spared-V1 topography as the V1/V2 border remained stable, and pRF eccentricity versus cortical-distance plots were similar to those of controls. Interestingly, three observations suggest limited reorganization: (i) the distribution of pRF centers in spared-V1 was shifted slightly toward the scotoma border in 2 of 5 patients compared with AS controls; (ii) pRF size in spared-V1 was slightly increased in patients near the scotoma border; and (iii) pRF size in the contralesional hemisphere was slightly increased compared with AS controls. Importantly, pRF measurements yield information about the functional properties of spared-V1 cortex not provided by standard perimetry mapping. In three patients, spared-V1 pRF maps overlapped significantly with dense regions of the perimetric scotoma, suggesting that pRF analysis may help identify visual field locations amenable to rehabilitation. Conversely, in the remaining two patients, spared-V1 pRF maps failed to cover sighted locations in the perimetric map, indicating the existence of V1-bypassing pathways able to mediate useful vision.Cortical damage of the visual pathway often results from posterior or middle cerebral artery infarcts, hemorrhages, and other brain injuries. The most common visual cortex lesions involve the primary visual cortex (V1), the chief relayer of visual information to higher visual areas. Damage to area V1 or its primary inputs leads to the loss of conscious vision in the corresponding region of the contralateral visual hemifield, producing a dense contralateral scotoma that often covers a hemifield (hemianopia) or a single visual field quadrant (quadrantanopia).A much-debated issue is whether the adult V1 is able to reorganize after injury. Reorganization refers to long-term changes in the neuronal circuit (1) and generally requires the growth of new anatomic connections or a permanent change in the strength of existing connections. Several studies report significant remapping in area V1 of patients suffering from macular degeneration and other retinal lesions (212). The extent of this remapping has recently been called into question, however (1, 1319). Less is known about how the visual system remaps to cover the visual field after injury to area V1 or its input projection from the lateral geniculate nucleus (LGN). Enlarged receptive fields have been found in areas surrounding chronic V1 lesions in cats (2022), and visual point spread functions were seen to enlarge over time in the areas surrounding focal V1 lesions in kittens (23). Smaller, short-term changes (2 d after the lesion) have been reported as well (24). As expected, reorganization is more extensive in young animals (23, 25) compared with adults (26). A change in the balance between excitation and inhibition may underlie this functional reorganization (2731).In humans, V1 injury is typically followed by a brief period of spontaneous recovery, which rarely lasts beyond 6 mo (32). Whether this recovery is the result of true visual system plasticity or is related to the gradual resolution of perilesional edema and general clinical improvement of the patients is unclear. A recent study in an adult human subject suggested that large-scale reorganization occurs in area V1 after partial deafferentiation by an optic radiation lesion (33); however, quantitative measurements were not performed. To date, there has been no systematic study in humans investigating how spared V1 cortex covers the visual field after chronic V1 injury. The present work is an effort in this direction.We used the population receptive field (pRF) mapping method (34) to study how spared area V1 covers the visual field after chronic injury in five adult human subjects suffering from partial or complete quadrantanopia. Our findings suggest that there is at best a limited degree of reorganization in the spared part of area V1 after partial V1 injury. Interestingly, the pattern of coverage of the visual field measured in spared V1 cortex by functional magnetic resonance imaging (fMRI) typically does not match predictions derived from perimetry maps. Identifying the patterns of mismatch and how they relate to the capacity of early visual areas to reorganize after injury will eventually allow the adoption of more rational strategies for visual rehabilitation.
Keywords:cortical blindness   quadrantanopia   plasticity   retinotopy   hemianopia
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