Early diffusion evidence of retrograde transsynaptic degeneration in the human visual system

Patel, Kevin R.; Ramsey, Lenny; Metcalf, Nicholas V.; Shulman, Gordon L.; Corbetta, Maurizio

doi:10.1212/wnl.0000000000002841

Cited by 16 publications

(8 citation statements)

References 35 publications

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“…This makes intuitive sense, as retrograde degeneration in humans is well underway and clearly evidenced by structural changes relatively early in the chronic period. 25 , 28 , 34 , 57 Intervening in the subacute period may catch the visual system in a state where degeneration is not yet complete. Therefore, we posit that future studies should investigate if early intervention in acute and sub-acute CB populations can slow the rate or magnitude of degeneration, keeping LI max closer to zero for longer and thus, further improving the potential for training induced visual recovery once participants reach the chronic poststroke period.…”

Section: Discussionmentioning

confidence: 99%

Optic Tract Shrinkage Limits Visual Restoration After Occipital Stroke

Fahrenthold

Cavanaugh

Jang

et al. 2021

Stroke

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Background and Purpose: Damage to the adult primary visual cortex (V1) causes vision loss in the contralateral visual hemifield, initiating a process of trans-synaptic retrograde degeneration. The present study examined functional implications of this process, asking if degeneration impacted the amount of visual recovery attainable from visual restoration training in chronic patients, and if restoration training impacted optic tract (OT) shrinkage. Methods: Magnetic resonance imaging was used to measure OT volumes bilaterally in 36 patients with unilateral occipital stroke. From OT volumes, we computed laterality indices (LI), estimating the stroke-induced OT shrinkage in each case. A subset of these chronic patients (n=14, 13±6 months poststroke) underwent an average of nearly 1 year of daily visual restoration training, which repeatedly stimulated vision in their blind field. The amount of visual field recovery was quantified using Humphrey perimetry, and post training magnetic resonance imaging was used to assess the impact of training on OT shrinkage. Results: OT LI was correlated with time since stroke: it was close to 0 (no measurable OT shrinkage) in subacute participants (<6 months poststroke) while chronic participants (>6 months poststroke) exhibited LI >0, but with significant variability. Visual training did not systematically alter LI, but chronic patients with baseline LI≈0 (no OT shrinkage) exhibited greater visual field recovery than those with LI>0. Conclusions: Unilateral OT shrinkage becomes detectable with magnetic resonance imaging by ≈7 months poststroke, albeit with significant interindividual variability. Although visual restoration training did not alter the amount of degeneration already sustained, OT shrinkage appeared to serve as a biomarker of the potential for training-induced visual recovery in chronic cortically blind patients.

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Section: Discussionmentioning

confidence: 99%

Optic Tract Shrinkage Limits Visual Restoration After Occipital Stroke

Fahrenthold

Cavanaugh

Jang

et al. 2021

Stroke

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“…Indeed, microstructural damage of the cortico-striatal and thalamo-cortical projections may result from mechanisms of retrograde [ 25 ] and anterograde [ 26 ] transneuronal axonal degeneration, respectively, caused by primary neurodegeneration of intermediate relay stations—mainly the substantia nigra—within the cortico-striatal-thalamo-cortical motor loop. In accordance with this speculation, similar alterations of DTI metrics have been demonstrated in the frontal WM of Parkinson’s disease (PD) patients [ 27 – 29 ].…”

Section: Discussionmentioning

confidence: 99%

Microstructural damage of the cortico-striatal and thalamo-cortical fibers in Fabry disease: a diffusion MRI tractometry study

et al. 2020

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Purpose Recent evidences have suggested the possible presence of an involvement of the extrapyramidal system in Fabry disease (FD), a rare X-linked lysosomal storage disorder. We aimed to investigate the microstructural integrity of the main tracts of the cortico-striatal-thalamo-cortical loop in FD patients. Methods Forty-seven FD patients (mean age = 42.3 ± 16.3 years, M/F = 28/21) and 49 healthy controls (mean age = 42.3 ± 13.1 years, M/F = 19/28) were enrolled in this study. Fractional anisotropy (FA), axial (AD), radial (RD), and mean diffusivity (MD) maps were computed for each subject, and connectomes were built using a standard atlas. Diffusion metrics and connectomes were then combined to carry on a diffusion MRI tractometry analysis. The main afferent and efferent pathways of the cortico-striatal-thalamo-cortical loop (namely, bundles connecting the precentral gyrus (PreCG) with the striatum and the thalamus) were evaluated. Results We found the presence of a microstructural involvement of cortico-striatal-thalamo-cortical loop in FD patients, predominantly affecting the left side. In particular, we found significant lower mean FA values of the left cortico-striatal fibers (p = 0.001), coupled to higher MD (p = 0.001) and RD (p < 0.001) values, as well as higher MD (p = 0.01) and RD (p = 0.01) values at the level of the thalamo-cortical fibers. Conclusion We confirmed the presence of an alteration of the extrapyramidal system in FD patients, in line with recent evidences suggesting the presence of brain changes as a possible reflection of the subtle motor symptoms present in this condition. Our results suggest that, along with functional changes, microstructural damage of this pathway is also present in FD patients.

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“…Damage to the optic radiations or primary visual cortex (V1) causes blindness in the contralesional visual hemifield of both eyes. Degeneration of ganglion cells in the retina has been detected following occipital lobe damage in postmortem studies [1 -3] and in in vivo studies [4][5][6] of monkeys, cats, and humans. Prior cross-sectional studies have shown that the distribution of retinal ganglion cell degeneration years after a stroke is spatially correlated with the persistent visual field defect [7][8][9].…”

Section: Introductionmentioning

confidence: 99%

Survival of retinal ganglion cells after damage to the occipital lobe in humans is activity dependent

et al. 2019

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Damage to the optic radiations or primary visual cortex leads to blindness in all or part of the contralesional visual field. Such damage disconnects the retina from its downstream targets and, over time, leads to trans-synaptic retrograde degeneration of retinal ganglion cells. To date, visual ability is the only predictor of retinal ganglion cell degeneration that has been investigated after geniculostriate damage. Given prior findings that some patients have preserved visual cortex activity for stimuli presented in their blind field, we tested whether that activity explains variability in retinal ganglion cell degeneration over and above visual ability. We prospectively studied 15 patients (four females, mean age = 63.7 years) with homonymous visual field defects secondary to stroke, 10 of whom were tested within the first two months after stroke. Each patient completed automated Humphrey visual field testing, retinotopic mapping with functional magnetic resonance imaging, and spectral-domain optical coherence tomography of the macula. There was a positive relation between ganglion cell complex (GCC) thickness in the blind field and early visual cortex activity for stimuli presented in the blind field. Furthermore, residual visual cortex activity for stimuli presented in the blind field soon after the stroke predicted the degree of retinal GCC thinning six months later. These findings indicate that retinal ganglion cell survival after ischaemic damage to the geniculostriate pathway is activity dependent.

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Early diffusion evidence of retrograde transsynaptic degeneration in the human visual system

Cited by 16 publications

References 35 publications

Optic Tract Shrinkage Limits Visual Restoration After Occipital Stroke

Optic Tract Shrinkage Limits Visual Restoration After Occipital Stroke

Microstructural damage of the cortico-striatal and thalamo-cortical fibers in Fabry disease: a diffusion MRI tractometry study

Survival of retinal ganglion cells after damage to the occipital lobe in humans is activity dependent

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