V1 Projection Zone Signals in Human Macular Degeneration Depend on Task, not Stimulus

Masuda, Yoichiro; Dumoulin, Serge O.; Nakadomari, Satoshi; Wandell, Brian A.

doi:10.1093/cercor/bhm256

Cited by 133 publications

(225 citation statements)

References 48 publications

(74 reference statements)

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“…It is important to note that none of these studies can measure the same neuron at multiple time points, but rather, they must sample from active neurons in similar locations, resulting in potential sampling biases that further complicate their interpretations (2,27). Similar conflicting measurements have been seen in human patients with bilateral foveal lesions from age-related macular degeneration, with some fMRI studies claiming extensive recovery within the V1 SPZ, whereas again, others showed no evidence for reorganization (7,18,35,(43)(44)(45).…”

Section: Comparisons With Studies On the Cortical Effects Of Other Rementioning

confidence: 98%

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

Barton

Brewer

2015

Proc. Natl. Acad. Sci. U.S.A.

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Are silencing, ectopic shifts, and receptive field (RF) scaling in cortical scotoma projection zones (SPZs) the result of long-term reorganization (plasticity) or short-term adaptation? Electrophysiological studies of SPZs after retinal lesions in animal models remain controversial, because they are unable to conclusively answer this question because of limitations of the methodology. Here, we used functional MRI (fMRI) visual field mapping through population RF (pRF) modeling with moving bar stimuli under photopic and scotopic conditions to measure the effects of the rod scotoma in human early visual cortex. As a naturally occurring central scotoma, it has a large cortical representation, is free of traumatic lesion complications, is completely reversible, and has not reorganized under normal conditions (but can as seen in rod monochromats). We found that the pRFs overlapping the SPZ in V1, V2, V3, hV4, and VO-1 generally (i) reduced their blood oxygen level-dependent signal coherence and (ii) shifted their pRFs more eccentric but (iii) scaled their pRF sizes in variable ways. Thus, silencing, ectopic shifts, and pRF scaling in SPZs are not unique identifiers of cortical reorganization; rather, they can be the expected result of short-term adaptation. However, are there differences between rod and cone signals in V1, V2, V3, hV4, and VO-1? We did not find differences for all five maps in more peripheral eccentricities outside of rod scotoma influence in coherence, eccentricity representation, or pRF size. Thus, rod and cone signals seem to be processed similarly in cortex. can adult human visual cortex reorganize after the removal of visual input?" This question can be studied through the effects of retinal lesions (causing scotomas), in which input from the retina has been removed, but cortical representations of the scotoma projection zone (SPZ) remain intact. Accordingly, emphasis must be placed on teasing apart effects of scotomas that relate to short-term cortical adaptation from those of long-term cortical plasticity (1) (terminology review is in ref.2). Here, we investigate this question in human cortex by using functional MRI (fMRI) to measure the immediate cortical SPZ responses in the unique paradigm of the naturally occurring rod scotoma.The photoreceptors in humans can be divided into two classes: cones, which are primarily responsible for vision under high-luminance (photopic) conditions, and rods, which are primarily responsible for vision under low-luminance (scotopic) conditions when the cones are inactive. The cones are an order of magnitude more highly concentrated in the fovea relative to the periphery, where they inform our most detailed visual experience (3). In contrast, the greatest concentrations of rods are more than ∼10°e ccentric from fixation and become increasingly sparse toward fixation until they are completely absent. This roughly circular rodfree zone covers a radius of ∼0.6-0.8°of visual angle about the fixation point (diameter = ∼1.25-1.7°) (4, 5). Under scotopic conditions, a...

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Section: Comparisons With Studies On the Cortical Effects Of Other Rementioning

confidence: 98%

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

Barton

Brewer

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Stimulating the occipital cortex of a patient blinded in adulthood by trauma to the optic nerves resulted in abnormal phosphene maps, also suggesting cortical remapping 17 . Despite these reports, the implication that remapping is responsible for the large-scale spread of activation within the lesion projection zone of patients with retinal lesions acquired in adulthood has been seriously questioned [18][19][20] .…”

Section: Introductionmentioning

confidence: 99%

Large-scale remapping of visual cortex is absent in adult humans with macular degeneration

et al. 2011

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International audienceThe occipital lobe contains a retinotopic representation of the visual field. The representation of the central retina in early visual areas (V1-3) is found at the occipital pole. When the central retina is lesioned in both eyes by macular degeneration, this region of visual cortex at the occipital pole is accordingly deprived of input. However, even when such lesions occur in adulthood, some visually driven activity in and around the occipital pole can be observed. It has been suggested that this activity is due to remapping of this area, so that it now responds to inputs from intact, peripheral retina. We evaluated whether or not remapping of visual cortex underlies this activity. Our fMRI results provide no evidence of remapping, questioning the contemporary view that early visual areas of the adult human brain have the capacity to reorganize extensively

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“…Several studies report significant remapping in area V1 of patients suffering from macular degeneration and other retinal lesions (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12). The extent of this remapping has recently been called into question, however (1,(13)(14)(15)(16)(17)(18)(19). 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).…”

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confidence: 99%

Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects

Papanikolaou

Keliris

Papageorgiou

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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 blindness | quadrantanopia | plasticity | retinotopy | hemianopia C ortical 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 (2-12). The extent of this remapping has recently been called into question, however (1,(13)(14)(15)(16)(17)(18)(19). Less is known about how the visual system remaps to cover the visual field after injury to a...

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V1 Projection Zone Signals in Human Macular Degeneration Depend on Task, not Stimulus

Cited by 133 publications

References 48 publications

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

Large-scale remapping of visual cortex is absent in adult humans with macular degeneration

Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects

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