Brain structure changes visualized in early- and late-onset blind subjects

doi:10.1016/j.neuroimage.2009.07.048

NeuroImage

Volume 49, Issue 1, 1 January 2010, Pages 134-140

https://doi.org/10.1016/j.neuroimage.2009.07.048 Get rights and content

Abstract

We examined 3D patterns of volume differences in the brain associated with blindness, in subjects grouped according to early and late onset. Using tensor-based morphometry, we mapped volume reductions and gains in 16 early-onset (EB) and 16 late-onset (LB) blind adults (onset < 5 and > 14 years old, respectively) relative to 16 matched sighted controls. Each subject's structural MRI was fluidly registered to a common template. Anatomical differences between groups were mapped based on statistical analysis of the resulting deformation fields revealing profound deficits in primary and secondary visual cortices for both blind groups. Regions outside the occipital lobe showed significant hypertrophy, suggesting widespread compensatory adaptations. EBs but not LBs showed deficits in the splenium and the isthmus. Gains in the non-occipital white matter were more widespread in the EBs. These differences may reflect regional alterations in late neurodevelopmental processes, such as myelination, that continue into adulthood.

Section snippets

Data acquisition

Subjects with no history of neurological, cognitive or sensorimotor deficits other than blindness participated in the study and were divided into two groups. The first group consisted of 16 early-onset blind individuals (with loss of vision before 5 years of age), aged between 19 and 55 years (mean age 36.2 ± 9.8 years; median age 36.0 years; 10 men, 6 women). The second group consisted of 16 late-onset blind subjects (i.e., with loss of vision after 14 years of age) aged between 22 and 56 years

Early-onset blindness: 3D maps

Early-blind subjects showed significant volume deficits in dorsal visual cortices, spanning both primary (BA 17) and secondary visual areas (BA 18, BA 19; Figs. 1, 2). Volumes were lower in occipital regions in both hemispheres, with more widespread deficits in the left hemisphere (asymmetry was not significant). Occipital regions showed large volume reductions, but differences were also detected elsewhere. Most notably, the cingulate region showed significant volume decreases, in both anterior

Discussion

Here we examined the 3D pattern of voxelwise volume differences in the brain associated with blindness, in groups of subjects stratified according to early and late onset. Widespread differences were found not only in brain regions closely associated with vision, but significant hypertrophy was detected in non-occipital areas.

Acknowledgments

This study was supported by grants from the Canadian Institutes of Health Research and by the Canada Research Chairs awarded to Franco Lepore and Maryse Lassonde. Madeleine Fortin was funded by the Fond de la Recherche en Santé du Québec and the Réseau de recherche en santé de la vision and Patrice Voss by the Natural Sciences and Engineering Research Council of Canada. Additional support for algorithm development was provided by the National Institute on Aging, the National Library of

References (50)

BlissI. et al.
Comparison of blind and sighted participants performance in a letter recognition working memory task
Brain Res. Cogn. Brain Res.
(2004)
ChiangM.C. et al.
3D pattern of brain atrophy in HIV/AIDS visualized using tensor-based morphometry
NeuroImage
(2007)
ChungM.K. et al.
A unified statistical approach to deformation-based morphometry
NeuroImage
(2001)
HoferS. et al.
Topography of the human corpus callosum revisited—comprehensive fiber tractography using diffusion tensor magnetic resonance imaging
NeuroImage
(2006)
NoppeneyU. et al.
Early visual deprivation induces structural plasticity in gray and white matter
Curr. Biol.
(2005)
RizzolattiG. et al.
The motor cortical system
Neuron
(2001)
RoderB. et al.
Memory for environmental sounds in sighted, congenitally and late blind adults: evidence for crossmodal compensation
Int. J. Psychophysiol.
(2003)
SchothF. et al.
Diffusion tensor imaging in acquired blind humans
Neurosci. Lett.
(2006)
TheoretH. et al.
Behavioral and neuroplastic changes in the blind: evidence for functionally relevant cross-modal interactions
J. Physiol. Paris
(2004)
WoodsR.P.
MultiTracer: a Java-based tool for anatomic delineation of grayscale volumetric images
NeuroImage
(2003)

YuC. et al.

Plasticity of the corticospinal tract in early blindness revealed by quantitative analysis of fractional anisotropy based on diffusion tensor tractography

NeuroImage

(2007)

AmediA. et al.

Early 'visual' cortex activation correlates with superior verbal memory in the blind

Nat. Neurosci.

(2003)

AmediA. et al.

Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects

Nat. Neurosci.

(2004)

Bro-Nielsen, M., Gramkow, C., 1996. Fast fluid registration of medical images. Proceedings of the 4th International...

BurtonH. et al.

Adaptive changes in early and late blind: a fMRI study of verb generation to heard nouns

J. Neurophysiol.

(2002)

ChristensenE.G. et al.

Deformable templates using large deformation kinematics

IEEE Trans. Image Process.

(1996)

CohenL.G. et al.

Functional relevance of cross-modal plasticity in blind humans

Nature

(1997)

CollignonO. et al.

Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects

Cereb. Cortex

(2007)

CollinsD.L. et al.

Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space

J. Comput. Assist. Tomogr.

(1994)

ElbertT. et al.

Increased cortical representation of the fingers of the left hand in string players

Science

(1995)

ElbertT. et al.

Expansion of the tonotopic area in the auditory cortex of the blind

J. Neurosci.

(2002)

FaillenotI. et al.

Visual working memory for shape and 3D-orientation: a PET study

NeuroReport

(1997)

FlorH. et al.

Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation

Nature

(1995)

Fortin, M., Voss, P., Lord, C., Lassonde, M., Pruessner, J., Saint-Amour, D., Lepore, F., 2008. Wayfinding in the...

GougouxF. et al.

A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals

PLOS Biol.

(2005)

Cited by (96)

Brain structural changes in blindness: a systematic review and an anatomical likelihood estimation (ALE) meta-analysis
2023, Neuroscience and Biobehavioral Reviews
In recent decades, numerous structural brain imaging studies investigated purported morphometric changes in early (EB) and late onset blindness (LB). The results of these studies have not yielded very consistent results, neither with respect to the type, nor to the anatomical locations of the brain morphometric alterations. To better characterize the effects of blindness on brain morphometry, we performed a systematic review and an Anatomical-Likelihood-Estimation (ALE) coordinate-based-meta-analysis of 65 eligible studies on brain structural changes in EB and LB, including 890 EB, 466 LB and 1257 sighted controls. Results revealed atrophic changes throughout the whole extent of the retino-geniculo-striate system in both EB and LB, whereas changes in areas beyond the occipital lobe occurred in EB only. We discuss the nature of some of the contradictory findings with respect to the used brain imaging methodologies and characteristics of the blind populations such as the onset, duration and cause of blindness. Future studies should aim for much larger sample sizes, eventually by merging data from different brain imaging centers using the same imaging sequences, opt for multimodal structural brain imaging, and go beyond a purely structural approach by combining functional with structural connectivity network analyses.
Impact of Prajñā yoga on cognition in adolescents with congenital and adventitious visual impairment
2022, Explore
Numerous scientific studies have investigated the impact of yoga on cognition in children and adults. However, fewer studies have assessed the impact of yogic practices on cognition in children and adolescents with visual impairment. Despite their keen intellectual abilities and advanced linguistic skills, teens with visual impairment often experience difficulties with cognitive control and behavioral regulation.
Memory plays an important role in cognition. Besides storing information, memory is also used for recall, defined as the retrieval of information the brain has recently been exposed to, and recognition, defined as the ability to recognize or retrieve the information previously encountered and stored in the brain.
The objective of the study was to observe the effectiveness of Prajñā Yoga on enhancing the cognition and verbal memory in adolescents with visual impairment. Degree of visual impairment and age of onset of visual impairment were considered while analyzing the study data.
An open-trial, single arm, pre–post study design was adopted. 273 adolescents with visual impairment were assessed across India using the Rey Auditory Verbal Learning Test (RAVLT), at baseline (before the intervention), immediately after the intervention, and at 40 days after the intervention. RAVLT measures recall and recognition through verbal memory.
Prajñā Yoga (PY) or the Art of Living Intuition Program is a unique intervention, based on ancient techniques of Pranayama, Super Brain Yoga, and Meditation, taught to children & adolescents between the ages 5 and 17.
The mean scores for Recognition (p=0.011) and Immediate recall (p=0.011) improved significantly after PY for the entire study population, regardless of the degree of visual impairment, gender and age of onset. A significant improvement in mean scores for Delayed Recall was seen after 40 days of daily practice (p = 0.007).
The functional characterization of callosal connections
2022, Progress in Neurobiology
The brain operates through the synaptic interaction of distant neurons within flexible, often heterogeneous, distributed systems. Histological studies have detailed the connections between distant neurons, but their functional characterization deserves further exploration. Studies performed on the corpus callosum in animals and humans are unique in that they capitalize on results obtained from several neuroscience disciplines. Such data inspire a new interpretation of the function of callosal connections and delineate a novel road map, thus paving the way toward a general theory of cortico-cortical connectivity. Here we suggest that callosal axons can drive their post-synaptic targets preferentially when coupled to other inputs endowing the cortical network with a high degree of conditionality. This might depend on several factors, such as their pattern of convergence-divergence, the excitatory and inhibitory operation mode, the range of conduction velocities, the variety of homotopic and heterotopic projections and, finally, the state-dependency of their firing. We propose that, in addition to direct stimulation of post-synaptic targets, callosal axons often play a conditional driving or modulatory role, which depends on task contingencies, as documented by several recent studies.
Review article: Structural brain alterations in prelingually deaf
2020, NeuroImage
Citation Excerpt :
Fig. 2 presents data from five studies that found regions with increased WM volume, FA, or AD in the deaf compared to hearing subjects. An increased WM volume in the deaf was found in the dorsal visual association cortex, right insula (Allen et al., 2008), and cerebellum (Leporé et al., 2010b). At the same time, increased FA was reported in the bilateral forceps major (Kim et al., 2009) and increased AD in the corpus callosum, left anterior thalamic radiation, and right corticospinal tract (Jiang et al., 2019).
Functional studies show that our brain has a remarkable ability to reorganize itself in the absence of one or more sensory modalities. In this review, we gathered all the available articles investigating structural alterations in congenitally deaf subjects. Some concentrated only on specific regions of interest (e.g., auditory areas), while others examined the whole brain. The majority of structural alterations were observed in the auditory white matter and were more pronounced in the right hemisphere. A decreased white matter volume or fractional anisotropy in the auditory areas were the most common findings in congenitally deaf subjects. Only a few studies observed alterations in the auditory grey matter. Preservation of the grey matter might be due to the cross-modal plasticity as well as due to the lack of sensitivity of methods used for microstructural alterations of grey matter. Structural alterations were also observed in the frontal, visual, and other cerebral regions as well as in the cerebellum. The observed structural brain alterations in the deaf can probably be attributed mainly to the cross-modal plasticity in the absence of sound input and use of sign instead of spoken language.
A sensitive period in the neural phenotype of language in blind individuals
2020, Developmental Cognitive Neuroscience
Citation Excerpt :
In humans, the inferior fronto-occipital fasciculus (IFOF) contains a set of fibers passing from the occipital lobe to the inferior frontal cortex, the inferior longitudinal fasciculus (ILF) connects the occipital to the anterior and medial temporal lobe, and the vertical occipital fasciculus (VOF) of Wernicke connects the ventral occipitotemporal cortex to the lateral occipito-parietal junction (Ashtari, 2012; Forkel et al., 2014; Yeatman et al., 2013). One possibility is that blindness from birth modifies the functional role of these tracts by changing the way language-related information is used by “visual” cortex (Atilgan et al., 2017; Hasson et al., 2016; Leporé et al., 2010). A recent neurocomputational model was proposed to explain how the functional pattern that is observed in blind individuals might emerge from a common sighted/blind architecture (Tomasello et al., 2019).
Congenital blindness modifies the neural basis of language: “visual” cortices respond to linguistic information, and fronto-temporal language networks are less left-lateralized. We tested the hypothesis that this plasticity follows a sensitive period by comparing the neural basis of sentence processing between adult-onset blind (AB, n = 16), congenitally blind (CB, n = 22) and blindfolded sighted adults (n = 18). In Experiment 1, participants made semantic judgments for spoken sentences and, in a control condition, solved math equations. In Experiment 2, participants answered “who did what to whom” yes/no questions for grammatically complex (with syntactic movement) and simpler sentences. In a control condition, participants performed a memory task with non-words. In both experiments, visual cortices of CB and AB but not sighted participants responded more to sentences than control conditions, but the effect was much larger in the CB group. Only the “visual” cortex of CB participants responded to grammatical complexity. Unlike the CB group, the AB group showed no reduction in left-lateralization of fronto-temporal language network, relative to the sighted. These results suggest that congenital blindness modifies the neural basis of language differently from adult-onset blindness, consistent with a developmental sensitive period hypothesis.
Organization of the commissural fiber system in congenital and late-onset blindness
2020, NeuroImage: Clinical
Citation Excerpt :
Although all studies concur on a volume reduction of the splenium, i.e. the posterior part of the corpus callosum, results regarding the other portions of the corpus callosum are inconclusive (Ptito et al., 2008; Tomaiuolo et al., 2014; Leporé et al., 2010; Levin et al., 2010; Bridge et al., 2009; Bock et al., 2013). For example, some authors have found an enlargement of the genu, the anterior portion of the corpus callosum (Ptito et al., 2008; Lepore et al., 2010), others an enlargement of the isthmus and the posterior part of the body (Tomaiuolo et al., 2014); still others found no changes at all in the anatomical organization of the corpus callosum (Bock et al., 2013). To the best of our knowledge, no studies have investigated the effects of blindness on the anterior commissure (AC) which is the second main component of the commissural system (Lamantia and Rakic, 1990).
We investigated the effects of blindness on the structural and functional integrity of the corpus callosum and the anterior commissure (AC), which together form the two major components of the commissural pathways. Twelve congenitally blind (CB), 15 late blind (LB; mean onset of blindness of 16.6 ± 8.9 years), and 15 matched normally sighted controls (SC) participated in a multimodal brain imaging study. Magnetic resonance imaging(MRI) data were acquired using a 3T scanner, and included a structural brain scan, resting state functional MRI, and diffusion-weighted imaging. We used tractography to divide the AC into its anterior (aAC) and posterior (pAC) branch. Virtual tract dissection was performed using a deterministic spherical deconvolution tractography algorithm. The corpus callosum was subdivided into five subregions based on the criteria described by Witelson and modified by Bermudez and Zatorre. Our data revealed decreased fractional anisotropy of the pAC in CB and LB compared to SC, together with an increase in the number of streamlines in CB only. In addition, the AC surface area was significantly larger in CB compared to SC and LB, and correlated with the number of streamlines in pAC (rho = 0.55) and tract volume (rho = 0.46). As for the corpus callosum, the splenial part was significantly smaller in CB and LB, and fewer streamlines passed through it. We did not find group differences in functional connectivity of cortical areas connected by fibers crossing any of the five callosal subregions. The present data suggest that the two main components of the commissural system undergo neuroplastic changes, irrespective of the age of onset of blindness, although the alterations observed in the AC are more important in congenital than late-onset blindness.

View all citing articles on Scopus

View full text

Brain structure changes visualized in early- and late-onset blind subjects

Abstract

Section snippets

Data acquisition

Early-onset blindness: 3D maps

Discussion

Acknowledgments

Brain Res. Cogn. Brain Res.

NeuroImage

NeuroImage

NeuroImage

Curr. Biol.

Neuron

Int. J. Psychophysiol.

Neurosci. Lett.

J. Physiol. Paris

NeuroImage

NeuroImage

Early 'visual' cortex activation correlates with superior verbal memory in the blind

Nat. Neurosci.

Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects

Nat. Neurosci.

Adaptive changes in early and late blind: a fMRI study of verb generation to heard nouns

J. Neurophysiol.

Deformable templates using large deformation kinematics

IEEE Trans. Image Process.

Functional relevance of cross-modal plasticity in blind humans

Nature

Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects

Cereb. Cortex

Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space

J. Comput. Assist. Tomogr.

Increased cortical representation of the fingers of the left hand in string players

Science

Expansion of the tonotopic area in the auditory cortex of the blind

J. Neurosci.

Visual working memory for shape and 3D-orientation: a PET study

NeuroReport

Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation

Nature

A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals

PLOS Biol.