Incomplete Cortical Reorganization in Macular Degeneration

Liu, Tingting; Cheung, Sing Hang; Schuchard, Ronald; Glielmi, Christopher; Hu, Xiaoping; He, Sheng; Legge, Gordon E.

doi:10.1167/iovs.09-4926

Cited by 60 publications

(85 citation statements)

References 21 publications

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“…Loss of central vision, for example, produces profound behavioral adaptation, although the neural bases of this adaptation remain controversial (e.g., refs. [34][35][36][37][38]. The mechanisms of long-term adaptation identified here may be similar to those that control this natural adaptation.…”

Section: Discussionmentioning

confidence: 57%

Distinct mechanism for long-term contrast adaptation

Bao

Engel

2012

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

113

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To optimize perception, neurons in the visual system adapt to the current environment. What determines the durability of this plasticity? Longer exposures to an environment produce longer-lasting effects, which could be due to either (i) a single mechanism controlling adaptation that gains strength over time, or (ii) long-term mechanisms that become active after long-term exposure. Using recently developed technology, we tested adaptation durations an order of magnitude greater that those tested previously, and used a "deadaptation" procedure to reveal effects of a unique long-term mechanism in the longest adaptation periods. After 4 h of contrast adaptation, human observers were exposed to natural images for 15 min, which completely cancelled perceptual aftereffects of adaptation. Strikingly, during continued testing this deadaptation faded, and the original adaptation effects reappeared. This pattern strongly suggests that adaptation was maintained in a distinct long-term mechanism, whereas deadaptation affected a short-term mechanism.orientation | deprivation | adult neuroplasticity T he visual system continually adapts to the current environment to improve its function. Neurons in the retina and visual cortex, for example, decrease their sensitivity after prolonged exposure to a high contrast environment (for reviews, see refs. 1 and 2). Such adaptation is hypothesized to increase the efficiency of neural coding by bringing responses down from ceiling levels and allowing neurons to respond differentially to the high contrast values that are the most likely stimuli in that environment. Because adaptation effects are both large and common in the natural world, understanding them is a key component of any account of visual function (3).Effects of contrast adaptation are evident almost immediately after onset of an adapting stimulus but get stronger and longerlasting as the adaptation period grows in duration. This duration scaling law has been observed for both firing rates of retinal ganglion cells and contrast detection measurements of human observers (4, 5).How the visual system produces these temporal dynamics remains the subject of debate (Fig. 1). One theory proposes that a single neural mechanism controls contrast adaptation at multiple time-scales (putting aside extremely rapid effects that occur within 100-200 ms; refs. 5 and 6). As the adapting period grows longer, this mechanism increases its confidence in its estimates of the current environment. Increased confidence, in turn, produces stronger adaptation effects and also increases the evidence required to convince the system that the environment has changed back to its original state, yielding longer-lasting aftereffects.Alternatively, contrast adaptation might be controlled by multiple neural mechanisms, each tuned to a different preferred timescale (7,8). As the adapting period grows longer, mechanisms tuned to longer timescales exert increased control over adaptation. The dynamics of such mechanisms would most naturally operate at similar long t...

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Section: Discussionmentioning

confidence: 57%

Distinct mechanism for long-term contrast adaptation

Bao

Engel

2012

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

113

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“…A combined fMRI and multi-unit neurophysiological study in a carefully controlled animal model (homonymous retinal, but not macular, lesions induced in adult macaques) also showed no long-term changes that would indicate remapping of visual cortex 25 . A recent report of a case series of four patients with age-related macular degeneration and four with the juvenile form also indicates limited reorganization, but explicit mapping experiments to assess group differences in cortical mapping quantitatively were not undertaken 43 .…”

Section: Discussionmentioning

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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“…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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Incomplete Cortical Reorganization in Macular Degeneration

Cited by 60 publications

References 21 publications

Distinct mechanism for long-term contrast adaptation

Distinct mechanism for long-term contrast adaptation

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

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

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