Several neuroimaging studies demonstrated that visual deprivation led to significant cross-modal plasticity in the brain’s functional and anatomical architecture.
Purpose
To investigate the pattern of the interhemispheric functional connectivity in individuals with late blindness using the voxel-mirrored homotopic connectivity (VMHC) and seed-based functional connectivity (FC) methods.
Material and Methods
Forty-four individuals with late blindness (22 men, 22 women; mean age = 39.88 ± 12.84 years) and 55 sighted control individuals (35 men, 20 women; mean age = 43.13 ± 13.98 years)—closely matched for age, sex, and education—underwent resting-state magnetic resonance imaging scans. The VMHC and seed-based FC methods were applied to assess interhemispheric coordination in a voxel-wise manner.
Results
Compared with the sighted control groups, the late blindness groups showed decreased VMHC values in the bilateral cuneus/calcarine/lingual gyrus (CUN/CAL/LING) (BA 17/18/19) (voxel level: P < 0.001, Gaussian random field [GRF] correction, cluster level: P < 0.005). Meanwhile, for seed-based FC analysis, compared with the sighted control group, the late blindness group showed a decreased FC between the right lower VMHC regions and the bilateral CUN/LING/CAL/precuneus (PreCUN)/left middle occipital gyrus (MOG) (BA 18/19/30/31) and left precentral gyrus (PreCG) and postcentral gyrus (PostCG) (BA 2/3/4/6). The late blindness group showed a decreased FC between the left lower VMHC regions and the bilateral CUN/LING/CAL/PreCUN (BA 18/19/31) and left PreCG and PostCG (BA 2/3/4/6) relative to the sighted control group (voxel level: P < 0.001, GRF correction, cluster level: P < 0.005). Moreover, a negative correlation was observed between the duration of blindness and VMHC values in the bilateral CUN/CAL/LING (r = −0.393, P = 0.008) in individuals with late blindness.
Conclusion
Our results indicated that late blindness induced substantial impairment of interhemispheric coordination in the visual cortex. This might reflect impaired visual fusion, visual recognition function, and top-down modulations in individuals with late blindness.
BurtonHMcLarenDG.Visual cortex activation in late-onset, Braille naive blind individuals: an fMRI study during semantic and phonological tasks with heard words.Neurosci Lett2006;
392:38–42.
2.
JiangFSteckerGCBoyntonGM, et al.
Early blindness results in developmental plasticity for auditory motion processing within auditory and occipital cortex.Front Hum Neurosci2016;
10:324.
3.
OfanRHZoharyE.Visual cortex activation in bilingual blind individuals during use of native and second language.Cereb Cortex2007;
17:1249–1259.
4.
MaurerDMondlochCJLewisTL.Effects of early visual deprivation on perceptual and cognitive development.Prog Brain Res2007;
164:87–104.
5.
CollignonODormalGAlbouyG, et al.
Impact of blindness onset on the functional organization and the connectivity of the occipital cortex.Brain2013;
136:2769–2783.
6.
KlingeCEippertFRöderB, et al.
Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind.J Neurosci2010;
30:12798–12805.
7.
BednyMPascual-LeoneADodell-FederD, et al.
Language processing in the occipital cortex of congenitally blind adults.Proc Natl Acad Sci USA2011;
108:4429–4434.
8.
CohenLGCelnikPPascual-LeoneA, et al.
Functional relevance of cross-modal plasticity in blind humans.Nature1997;
389:180–183.
9.
YuCLiuYLiJ, et al.
Altered functional connectivity of primary visual cortex in early blindness.Hum Brain Mapp2008;
29:533–543.
10.
WittenbergGFWerhahnKJWassermannEM, et al.
Functional connectivity between somatosensory and visual cortex in early blind humans.Eur J Neurosci2004;
20:1923–1927.
11.
PellandMOrbanPDansereauC, et al.
State-dependent modulation of functional connectivity in early blind individuals.Neuroimage2017;
147:532–541.
12.
SabbahNAuthiéCNSandaN, et al.
Increased functional connectivity between language and visually deprived areas in late and partial blindness.Neuroimage2016;
136:162–173.
13.
CoullonGSJiangFFineI, et al.
Subcortical functional reorganization due to early blindness.J Neurophysiol2015;
113:2889–2899.
14.
PtitoMSchneiderFCPaulsonOB, et al.
Alterations of the visual pathways in congenital blindness.Exp Brain Res2008;
187:41–49.
15.
ReislevNHDyrbyTBSiebnerHR, et al.
Thalamocortical connectivity and microstructural changes in congenital and late blindness.Neural Plast2017;2017:9807512.
16.
EngelAKKönigPKreiterAK, et al.
Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex.Science1991;
252:1177–1179.
17.
MizunoHHiranoTTagawaY.Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity.J Neurosci2007;
27:6760–6770.
18.
ButtOHBensonNCDattaR, et al.
Hierarchical and homotopic correlations of spontaneous neural activity within the visual cortex of the sighted and blind.Front Hum Neurosci2015;
9:25.
19.
TagawaYMizunoHHiranoT.Activity-dependent development of interhemispheric connections in the visual cortex.Rev Neurosci2008;
19:19–28.
20.
HouFLiuXZhouZ, et al.
Reduction of interhemispheric functional brain connectivity in early blindness: a resting-state fMRI study.Biomed Res Int2017;
2017:6756927.
21.
TomaiuoloFCampanaSCollinsDL, et al.
Morphometric changes of the corpus callosum in congenital blindness.PLoS One2014;
9:e107871.
22.
ShiJCollignonOXuL, et al.
Impact of early and late visual deprivation on the structure of the corpus callosum: a study combining thickness profile with surface tensor-based morphometry.Neuroinformatics2015;
13:321–336.
23.
TeradaKUsuiNUmeokaS, et al.
Interhemispheric connection of motor areas in humans.J Clin Neurophysiol2008;
25:351–356.
24.
BernasconiFGrivelJMurrayMM, et al.
Interhemispheric coupling between the posterior sylvian regions impacts successful auditory temporal order judgment.Neuropsychologia2010;
48:2579–2585.
25.
MimaTOluwatimilehinTHiraokaT, et al.
Transient interhemispheric neuronal synchrony correlates with object recognition.J Neurosci2001;
21:3942–3948.
26.
StarkDEMarguliesDSShehzadZE, et al.
Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations.J Neurosci2008;
28:13754–13764.
27.
ZuoXNKellyCDi MartinoA, et al.
Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy.J Neurosci2010;
30:15034–15043.
28.
YanCQLiuCZWangX, et al.
Abnormal functional connectivity of anterior cingulate cortex in patients with primary insomnia: a resting-state functional magnetic resonance imaging study.Front Aging Neurosci2018;
10:167.
29.
ZhaoLWangYJiaY, et al.
Altered interhemispheric functional connectivity in remitted bipolar disorder: a resting state fMRI study.Sci Rep2017;
7:4698.
30.
HouZSuiYSongX, et al.
Disrupted interhemispheric synchrony in default mode network underlying the impairment of cognitive flexibility in late-onset depression.Front Aging Neurosci2016;
8:230.
31.
YanCGWangXDZuoXN, et al.
DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging.Neuroinformatics2016;
14:339–351.
32.
Van DijkKRSabuncuMRBucknerRL.The influence of head motion on intrinsic functional connectivity MRI.Neuroimage2012;
59:431–438.
33.
GotoMAbeOAokiS, et al.
Diffeomorphic Anatomical Registration Through Exponentiated Lie Algebra provides reduced effect of scanner for cortex volumetry with atlas-based method in healthy subjects.Neuroradiology2013;
55:869–875.
34.
SongXWDongZYLongXY, et al.
REST: a toolkit for resting-state functional magnetic resonance imaging data processing.PLoS One2011;
6:e25031.
35.
RaemaekersMSchellekensWvan WezelRJ, et al.
Patterns of resting state connectivity in human primary visual cortical areas: a 7T fMRI study.Neuroimage2014;
84:911–921.
36.
LuKHJeongJYWenH, et al.
Spontaneous activity in the visual cortex is organized by visual streams.Hum Brain Mapp2017;
38:4613–4630.
37.
GotoYTaniwakiTKinukawaN, et al.
Interhemispheric functional synchronization at the first step of visual information processing in humans.Clin Neurophysiol2004;
115:1409–1416.
38.
MimaTOluwatimilehinTHiraokaT, et al.
Transient interhemispheric neuronal synchrony correlates with object recognition.J Neurosci2001;
21:3942–3948.
39.
BerardiNBodis-WollnerIFiorentiniA, et al.
Electrophysiological evidence for interhemispheric transmission of visual information in man.J Physiol1989;
411:207–225.
40.
RochefortNLBuzásPQuenech’duN, et al.
Functional selectivity of interhemispheric connections in cat visual cortex.Cereb Cortex2009;
19:2451–2465.
41.
MilleretCHouzelJC.Visual interhemispheric transfer to areas 17 and 18 in cats with convergent strabismus.Eur J Neurosci2001;
13:137–152.
42.
SingerW.Consciousness and the structure of neuronal representations.Philos Trans R Soc Lond B Biol Sci1998;
353:1829–1840.
43.
VeraartCDe VolderAGWanet-DefalqueMC, et al.
Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset.Brain Res1990;
510:115–121.
44.
QinWXuanYLiuY, et al.
Functional connectivity density in congenitally and late blind subjects.Cereb Cortex2015;
25:2507–2516.
45.
LiuYYuCLiangM, et al.
Whole brain functional connectivity in the early blind.Brain2007;
130:2085–2096.
46.
PtitoMSchneiderFCPaulsonOB, et al.
Alterations of the visual pathways in congenital blindness.Exp Brain Res2008;
187:41–49.
47.
Rita MachadoACarvalho PereiraAFerreiraF, et al.
Structure-function correlations in Retinitis Pigmentosa patients with partially preserved vision: a voxel-based morphometry study.Sci Rep2017;
7:11411.
48.
GazzanigaMS.Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition?Brain2000;
123:1293–1326.
49.
RolandJLSnyderAZHackerCD, et al.
On the role of the corpus callosum in interhemispheric functional connectivity in humans.Proc Natl Acad Sci USA2017;
114:13278–13283.
50.
ShimonyJSBurtonHEpsteinAA, et al.
Diffusion tensor imaging reveals white matter reorganization in early blind humans.Cereb Cortex2006;
16:1653–1661.
51.
GilbertCDLiW.Top-down influences on visual processing.Nat Rev Neurosci2013;
14:350–363.
52.
LuKHJeongJYWenH, et al.
Spontaneous activity in the visual cortex is organized by visual streams.Hum Brain Mapp2017;
38:4613–4630.
53.
WangKJiangTYuC, et al.
Spontaneous activity associated with primary visual cortex: a resting-state FMRI study.Cereb Cortex2008;
18:697–704.
54.
KosslynSMThompsonWLKimIJ, et al.
Topographical representations of mental images in primary visual cortex.Nature1995;
378:496–498.
55.
D’EspositoMDetreJAAguirreGK, et al.
A functional MRI study of mental image generation.Neuropsychologia1997;
35:725–730.
56.
DaiHMorelliJNAiF, et al.
Resting-state functional MRI: functional connectivity analysis of the visual cortex in primary open-angle glaucoma patients.Hum Brain Mapp2013;
34:2455–2463.
57.
MurphyMCNauACFisherC, et al.
Top-down influence on the visual cortex of the blind during sensory substitution.Neuroimage2016;
125:932–940.
58.
KruseWDannenbergSKleiserR, et al.
Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements.Cereb Cortex2002;
12:466–476.
59.
BurtonHSnyderAZRaichleME.Resting state functional connectivity in early blind humans.Front Syst Neurosci2014;
8:51.
60.
CunninghamSIWeilandJDBaoP, et al.
Correlation of vision loss with tactile-evoked V1 responses in retinitis pigmentosa.Vision Res2015;
111:197–207.
