Lack of long-term cortical reorganization after macaque retinal lesions

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...

Section: Resultsmentioning

confidence: 99%

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

confidence: 99%

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

confidence: 99%

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

Barton

Brewer

2015

“…The brain matures in a sequential manner in which some circuits develop and stabilize while others remain capable of plastic change (51)(52)(53)(54). In this view, reading instruction should be delivered when the systems needed to learn .…”

Section: Discussionmentioning

confidence: 99%

Development of white matter and reading skills

Yeatman

Dougherty

Ben-Shachar

et al. 2012

294

356

White matter tissue properties are highly correlated with reading proficiency; we would like to have a model that relates the dynamics of an individual's white matter development to their acquisition of skilled reading. The development of cerebral white matter involves multiple biological processes, and the balance between these processes differs between individuals. Cross-sectional measures of white matter mask the interplay between these processes and their connection to an individual's cognitive development. Hence, we performed a longitudinal study to measure white-matter development (diffusion-weighted imaging) and reading development (behavioral testing) in individual children (age 7-15 y). The pattern of white-matter development differed significantly among children. In the left arcuate and left inferior longitudinal fasciculus, children with above-average reading skills initially had low fractional anisotropy (FA) that increased over the 3-y period, whereas children with belowaverage reading skills had higher initial FA that declined over time. We describe a dual-process model of white matter development comprising biological processes with opposing effects on FA, such as axonal myelination and pruning, to explain the pattern of results.R eading requires efficient communication within a network of visual, auditory, and language-processing regions that are separated by many centimeters. Hence, the white-matter fascicles that connect these regions are critical for proficient reading (1). Only in the last decade has it become possible to study the microstructural properties of the white matter in the living human brain, and only in recent years has there been an opportunity to trace the developmental progression of these fascicles systematically. During this decade it has been shown that learning to read is associated with corresponding changes in sensory and language circuits in the brain (2-5).Diffusion measurements of the white-matter pathways (3, 5-7) and neurological case studies (8, 9) suggest that in typical development and education both the left hemisphere arcuate fasciculus and inferior longitudinal fasciculus (ILF) carry signals important for reading. Studies in adults, adolescents, and schoolage children have reported differences between good and poor readers in white-matter volume and diffusion properties in the vicinity of these pathways (10-14). One possibility is that these differences are present from an early age, remain constant through development, and constrain children's aptitude for reading. An alternative possibility is that there is an interaction between the biological development and timing of instruction. Two case studies support this hypothesis. When damage to the arcuate fasciculus occurs at birth, normal reading skills can develop (15); when damage to the arcuate fasciculus occurs later, for example after reading instruction has begun, it can result in severe reading impairment (9). These cases suggest that learning depends on the circuits' current state and capacity for plasti...

“…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).…”

mentioning

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

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...