A quantitative analysis of the retinofugal projections in congenital and late-onset blindness

[en] Vision loss early in life has dramatic consequences on the organization of the visual system and hence on structural plasticity of its remnant components. Most of the studies on the anatomical changes in the brain following visual deprivation have focused on the re-organization of the visual cortex and its afferent and efferent projections. In this study, we performed a quantitative analysis of the volume and size of the optic chiasm, optic nerve, optic tract and the lateral geniculate nucleus (LGN), the retino recipient thalamic nucleus. Analysis was carried out on structural T1-weighted MRIs from 22 congenitally blind (CB), 14 late blind (LB) and 29 age -and sex-matched sighted control (SC) subjects. We manually segmented the optic nerve, optic chiasm and optic tract, while LGN volumes were extracted using in-house software. We also measured voxel intensity of optic nerve, optic chiasm and optic tract. Mean volumes of the optic nerve, optic tract and optic chiasm were reduced by 50 to 60% in both CB and LB participants. No significant differences were found between the congenitally and late-onset blind participants for any of the measures. Our data further revealed reduced white matter voxel intensities in optic nerve, optic chiasm and optic tract in blind compared to sighted participants, suggesting decreased myelin content in the atrophied white matter. The LGN was reduced by 50% and 44% in CB and LB, respectively. In LB, optic nerve volume correlated negatively with the blindness duration index; no such correlation was found for optic chiasm, optic tract and LGN. The observation that despite the absence of visual input about half of the subcortical retinofugal projections are structurally preserved raises the question of their functional role. One possibility is that the surviving fibers play a role in the maintenance of circadian rhythms in the blind through the intrinsically photosensitive melanopsin-containing retinal ganglion cells. © 2021

Disciplines :

Neurosciences & behavior

Author, co-author :

Ptito, M.; School of Optometry, University of Montreal, Montreal, QC, Canada, BRAINlab, University of Copenhagen, Copenhagen, Denmark, Danish Research Center for Magnetic Resonance (DRCMR), Copenhagen University Hospital, Hvidovre, Denmark

Paré, S.; School of Optometry, University of Montreal, Montreal, QC, Canada

Dricot, L.; Institute of NeuroScience (IoNS), Université catholique de Louvain (UCLouvain), Belgium

Cavaliere, Carlo ; Université de Liège - ULiège > GIGA

Tomaiuolo, F.; Univesità degli Studi di Messina, Dipartimento di Medicina Clinica e Sperimentale

Kupers, R.; School of Optometry, University of Montreal, Montreal, QC, Canada, BRAINlab, University of Copenhagen, Copenhagen, Denmark, Institute of NeuroScience (IoNS), Université catholique de Louvain (UCLouvain), Belgium

Language :

English

Title :

A quantitative analysis of the retinofugal projections in congenital and late-onset blindness

Publication date :

2021

Journal title :

NeuroImage: Clinical

eISSN :

2213-1582

Publisher :

Elsevier Inc.

Volume :

Issue :

January

Pages :

102809

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Københavns Universitet, KU; Lundbeckfonden

Available on ORBi :

since 01 October 2021

Statistics

Number of views

32 (4 by ULiège)

Number of downloads

4 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Abbott, C.W., Kozanian, O.O., Huffman, K.J., The effects of lifelong blindness on murine neuroanatomy and gene expression. Front. Aging Neurosci., 7, 2015, 144.
Andrews, T.J., Halpern, S.D., Purves, D., Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 17 (1997), 2859–2868.
Aubin, S., Christensen, J.A., Jennum, P., Nielsen, T., Kupers, R., Ptito, M., Preserved sleep microstructure in blind individuals. Sleep Med. 42 (2018), 21–30.
Aubin, S., Gacon, C., Jennum, P., Ptito, M., Kupers, R., Altered sleep–wake patterns in blindness: a combined actigraphy and psychometric study. Sleep Med. 24 (2016), 100–108.
Aubin, S., Kupers, R., Ptito, M., Jennum, P., Melatonin and cortisol profiles in the absence of light perception. Behav. Brain Res. 317 (2017), 515–521.
Beatty, R.M., Sadun, A.A., Smith, L.E.H., Vonsattel, J.P., Richardson, E.P., Direct demonstration of transsynaptic degeneration in the human visual system: a comparison of retrograde and anterograde changes. J. Neurol. Neurosurg. Psychiatry 45 (1982), 143–146.
Bedny, M., Pascual-Leone, A., Dodell-Feder, D., Fedorenko, E., Saxe, R., Language processing in the occipital cortex of congenitally blind adults. Proc. Natl. Acad. Sci. 108 (2011), 4429–4434.
Bottomley, P.A., Hart, H.R. Jr, Edelstein, W.A., Schenck, J.F., Smith, L.S., Leue, W.M., Mueller, O.M., Redington, R.W., Anatomy and metabolism of the normal human brain studied by magnetic resonance at 1.5 Tesla. Radiology 150 (1984), 441–446.
Breitenseher, M., Uhl, F., Wimberger, D.P., Deecke, L., Trattnig, S., Kramer, J., Morphological dissociation between visual pathways and cortex: MRI of visually-deprived patients with congenital peripheral blindness. Neuroradiology 40 (1998), 424–427.
Bridge, H., Jindahra, P., Barbur, J., Plant, G.T., Imaging reveals optic tract degeneration in hemianopia. Invest. Ophthalmol. Vis. Sci. 52 (2011), 382–388.
Burgel, U., Amunts, K., Hoemke, L., Mohlberg, H., Gilsbach, J.M., Zilles, K., White matter fiber tracts of the human brain: threedimensional mapping at microscopic resolution, topography and intersubject variability. NeuroImage 29 (2006), 1092–1105.
Butt, O.H., Benson, N.C., Datta, R., Aguirre, G.K., The fine-scale functional correlation of striate cortex in sighted and blind people. J. Neurosci. 33 (2013), 16209–16219.
Cavaliere, C., Aiello, M., Soddu, A., Laureys, S., Reislev, N.L., Ptito, M., Kupers, R., Organization of the commissural fiber system in congenital and late-onset blindness. Neuroimage Clin., 25, 2020, 102133, 10.1016/j.nicl.2019.102133.
Cecchetti, L., Ricciardi, E., Handjaras, G., Kupers, R., Ptito, M., Pietrini, P., Congenital blindness affects diencephalic but not mesencephalic structures in the human brain. Brain Struct. Funct. 221 (2016), 1465–1480.
Chabot, N., Charbonneau, V., Laramée, M.-E., Tremblay, R., Boire, D., Bronchti, G., Subcortical auditory input to the primary visual cortex in anophthalmic mice. Neurosci. Lett. 433 (2008), 129–134.
Charbonneau, V., Laramée, M.-E., Boucher, V., Bronchti, G., Boire, D., Cortical and subcortical projections to primary visual cortex in anophthalmic, enucleated and sighted mice. Eur. J. Neurosci. 36 (2012), 2949–2963.
Desgent, S., Ptito, M., Cortical GABAergic interneurons in cross-modal plasticity following early blindness. Neural Plast., 2012, 2012, 590725, 10.1155/2012/590725.
Eickhoff, S.B., Stephan, K.E., Mohlberg, H., Grefkes, C., Fink, G.R., Amunts, K., Zilles, K., A. new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25 (2005), 1325–1335.
Farnum, A., Pelled, G., New Vision for Visual Prostheses. Front. Neurosci., 14, 2020, 10.3389/fnins.2020.00036.
Fernandez, E., Development of visual Neuroprostheses: trends and challenges. Bioelectron. Med., 4, 2018, 12.
Fortin, M., Voss, P., Lord, C., Lassonde, M., Pruessner, J., Saint-Amour, D., Rainville, C., Lepore, F., Wayfinding in the blind: larger hippocampal volume and supranormal spatial navigation. Brain 131 (2008), 2995–3005.
Frezzotti, P., Giorgio, A., Motolese, I., De Leucio, A., Iester, M., Motolese, E., Federico, A., De Stefano, N., Structural and functional brain changes beyond visual system in patients with advanced glaucoma. PLoS One, 9, 2014, e105931.
Gupta, N., Greenberg, G., De Tilly, L.N., Gray, B., Polemidiotis, M., Yücel, Y.H., Atrophy of the lateral geniculate nucleus in human glaucoma detected by magnetic resonance imaging. Br. J. Ophthalmol. 93 (2009), 56–60.
Hagiwara, A., Hori, M., Kamagata, K., Warntjes, M., Matsuyoshi, D., Nakazawa, M., Ueda, R., Andica, C., Koshino, S., Maekawa, T., Myelin measurement: Comparison between simultaneous tissue relaxometry, magnetization transfer saturation index, and T 1 w/T 2 w ratio methods. Sci. Rep. 8 (2018), 1–12.
Heine, L., Bahri, M.A., Cavaliere, C., Soddu, A., Laureys, S., Ptito, M., Prevalence of increases in functional connectivity in visual, somatosensory and language areas in congenital blindness. Front. Neuroanat., 9, 2015, 86.
Hernowo, A.T., Boucard, C.C., Jansonius, N.M., Hooymans, J.M., Cornelissen, F.W., Automated morphometry of the visual pathway in primary open-angle glaucoma. Invest Ophthalmol Vis Sci 52 (2011), 2758–2766.
Hickey, T.L., Guillery, R.W., Variability of laminar patterns in the human lateral geniculate nucleus. J. Comp. Neurol. 183 (1979), 221–246.
Hoffmann, M.B., Dumoulin, S.O., Congenital visual pathway abnormalities: a window onto cortical stability and plasticity. Trends Neurosci. 38 (2015), 55–65.
Jiang, J., Zhu, W., Shi, F., Liu, Y., Li, J., Qin, W., Li, K., Yu, C., Jiang, T., Thick visual cortex in the early blind. J. Neurosci. 29 (2009), 2205–2211.
Karlen, S.J., Kahn, D.M., Krubitzer, L., Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience 142 (2006), 843–858.
Kelly, K.R., McKetton, L., Schneider, K.A., Gallie, B.L., Steeves, J.K., Altered anterior visual system development following early monocular enucleation. Neuroimage Clinical 4 (2013), 72–81.
Kelter, R., Bayesian alternatives to null hypothesis significance testing in biomedical research: a non-technical introduction to Bayesian inference with JASP. BMC Med. Res. Methodol. 20 (2020), 1–12.
Keysers, C., Gazzola, V., Wagenmakers, E.-J., Using Bayes factor hypothesis testing in neuroscience to establish evidence of absence. Nat. Neurosci. 23:7 (2020), 788–799.
Kosior-Jarecka, E., Pankowska, A., Polit, P., Stępniewski, A., Symms, M.R., Kozioł, P., Żarnowski, T., Pietura, R., Volume of lateral geniculate nucleus in patients with glaucoma in 7Tesla MRI. J. Clin. Med., 9, 2020, 2382.
Kozanian, O.O., Abbott, C.W., Huffman, K.J., Rapid changes in cortical and subcortical brain regions after early bilateral enucleation in the mouse. PLoS One, 10, 2015, e0140391, 10.1371/journal.pone.0140391.
Krug, K., Principles of function in the visual system. Sensory Perception, 2012, Springer, 41–56.
Kupers, R., Ptito, M., Structural, metabolic and functional changes in the congenitally blind brain. Int. J. Psychophysiol., 2, 2014, 152.
Kupers, R., Ptito, M., Compensatory plasticity and cross-modal reorganization following early visual deprivation. Neurosci. Biobehav. Rev. 41 (2014), 36–52.
Lee, J.Y., Jeong, H.J., Lee, J.H., Kim, Y.J., Kim, E.Y., Kim, Y.Y., Ryu, T., Cho, Z.-H., Kim, Y.-B., An investigation of lateral geniculate nucleus volume in patients with primary open-angle glaucoma using 7 tesla magnetic resonance imaging. Invest. Ophthalmol. Vis. Sci. 55 (2014), 3468–3476.
Lee, M.D., Wagenmakers, E.-J., Bayesian Cognitive Modeling: A Practical Course. 2014, Cambridge University Press.
Liu, Y., Yu, C., Liang, M., Li, J., Tian, L., Zhou, Y., Qin, W., Li, K., Jiang, T., Whole brain functional connectivity in the early blind. Brain 130 (2007), 2085–2096.
Maeda, A., Mandai, M., Takahashi, M., Gene and induced pluripotent stem cell therapy for retinal diseases. Annu. Rev. Genomics Hum. Genet. 20 (2019), 201–216.
Manara, R., Citton, V., Maffei, P., Marshall, J.D., Naggert, J.K., Milan, G., Vettor, R., Baglione, A., Vitale, A., Briani, C., Degeneration and plasticity of the optic pathway in Alström syndrome. Am. J. Neuroradiol. 36 (2015), 160–165.
Mcketton, L., Kelly, K.R., Schneider, K.A., Abnormal lateral geniculate nucleus and optic chiasm in human albinism. J. Comp. Neurol. 522 (2014), 2680–2687.
Meaidi, A., Jennum, P., Ptito, M., Kupers, R., The sensory construction of dreams and nightmare frequency in congenitally blind and late blind individuals. Sleep Med. 15 (2014), 586–595.
Mirochnik, R.M., Pezaris, J.S., Contemporary approaches to visual prostheses. Mil. Med. Res., 6, 2019, 19, 10.1186/s40779-019-0206-9.
Müller, F., Niso, G., Samiee, S., Ptito, M., Baillet, S., Kupers, R., A thalamocortical pathway for fast rerouting of tactile information to occipital cortex in congenital blindness. Nat. Commun. 10 (2019), 1–9.
Noppeney, U., The effects of visual deprivation on functional and structural organization of the human brain. Neurosci. Biobehav. Rev. 31 (2007), 1169–1180.
Ogawa, S., Takemura, H., Horiguchi, H., Terao, M., Haji, T., Pestilli, F., Yeatman, J.D., Tsuneoka, H., Wandell, B.A., Masuda, Y., White matter consequences of retinal receptor and ganglion cell damage. Invest. Ophthalmol. Vis. Sci. 55 (2014), 6976–6986.
Pan, W.-J., Wu, G., Li, C.-X., Lin, F., Sun, J., Lei, H., Progressive atrophy in the optic pathway and visual cortex of early blind Chinese adults: a voxel-based morphometry magnetic resonance imaging study. Neuroimage 37 (2007), 212–220.
Papadopoulou, A., Gaetano, L., Pfister, A., Altermatt, A., Tsagkas, C., Morency, F., Brandt, A.U., Hardmeier, M., Chakravarty, M.M., Descoteaux, M., Damage of the lateral geniculate nucleus in MS: Assessing the missing node of the visual pathway. Neurology 92 (2019), e2240–e2249.
Ptito, M., Bleau, M., Djerourou, I., Paré, S., Schneider, F.C., Chebat, D.-R., Brain-machine interfaces to assist the blind. Front. Hum. Neurosci., 15, 2021, 46.
Ptito, M., Schneider, F.C., Paulson, O.B., Kupers, R., Alterations of the visual pathways in congenital blindness. Exp. Brain Res. 187 (2008), 41–49.
Reislev, Kupers, R., Siebner, H.R., Ptito, M., Dyrby, T.B., Blindness alters the microstructure of the ventral but not the dorsal visual stream. Brain Struct. Funct. 221 (2016), 2891–2903.
Reislev, N.H., Dyrby, T.B., Siebner, H.R., Lundell, H., Ptito, M., Kupers, R., Thalamocortical connectivity and microstructural changes in congenital and late blindness. Neural Plast., 2017, 2017, 9807512, 10.1155/2017/9807512.
Reislev, N.H., Dyrby, T.B., Siebner, H.R., Kupers, R., Ptito, M., Simultaneous assessment of white matter changes in microstructure and connectedness in the blind brain. Neural Plast., 2016, 2016, 6029241, 10.1155/2016/6029241.
Rizzo, G., Tozer, K.R., Tonon, C., Manners, D., Testa, C., Malucelli, E., Valentino, M.L., La Morgia, C., Barboni, P., Randhawa, R.S., Secondary post-geniculate involvement in Leber's hereditary optic neuropathy. PLoS One, 7, 2012, e50230.
Rovsing, L., Rath, M.F., Lund-Andersen, C., Klein, D.C., Møller, M., A neuroanatomical and physiological study of the non-image forming visual system of the cone-rod homeobox gene (Crx) knock out mouse. Brain Res. 1343 (2010), 54–65.
Schmidt, M.A., Knott, M., Heidemann, R., Michelson, G., Kober, T., Dörfler, A., Engelhorn, T., Investigation of lateral geniculate nucleus volume and diffusion tensor imaging in patients with normal tension glaucoma using 7 tesla magnetic resonance imaging. PLoS One, 13, 2018, e0198830.
Schmitz, B., Schaefer, T., Krick, C.M., Reith, W., Backens, M., Käsmann-Kellner, B., Configuration of the optic chiasm in humans with albinism as revealed by magnetic resonance imaging. Invest. Ophthalmol. Vis. Sci. 44 (2003), 16–21.
Shimony, J.S., Burton, H., Epstein, A.A., McLaren, D.G., Sun, S.W., Snyder, A.Z., Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb. Cortex 16 (2006), 1653–1661.
Tomaiuolo, F., Campana, S., Collins, D.L., Fonov, V.S., Ricciardi, E., Sartori, G., Pietrini, P., Kupers, R., Ptito, M., Morphometric changes of the corpus callosum in congenital blindness. PLoS One, 9, 2014, e107871.
Tomaiuolo, F., Di Paola, M., Caravale, B., Vicari, S., Petrides, M., Caltagirone, C., Morphology and morphometry of the corpus callosum in Williams syndrome: a T1-weighted MRI study. Neuroreport 13 (2002), 2281–2284.
Wang, D., Qin, W., Liu, Y., Zhang, Y., Jiang, T., Yu, C., Altered white matter integrity in the congenital and late blind people. Neural Plast., 2013, 2013, 128236, 10.1155/2013/128236.
Watkins, K.E., Shakespeare, T.J., O'Donoghue, M.C., Alexander, I., Ragge, N., Cowey, A., Bridge, H., Early auditory processing in area V5/MT+ of the congenitally blind brain. J. Neurosci. 33 (2013), 18242–18246.
You, Y., Gupta, V.K., Graham, S.L., Klistorner, A., Anterograde degeneration along the visual pathway after optic nerve injury. PLoS One, 7, 2012, e52061.
Zaidi, F.H., Hull, J.T., Peirson, S.N., Wulff, K., Aeschbach, D., Gooley, J.J., Brainard, G.C., Gregory-Evans, K., Rizzo, J.F. III, Czeisler, C.A., Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr. Biol. 17 (2007), 2122–2128.