Visual Cortex Alterations in Early and Late Blind Subjects During Tactile Perception

Abstract

Involvement of visual cortex varies during tactile perception tasks in early blind (EB) and late blind (LB) human subjects. This study explored differences in sensory motor networks associated with tactile task in EB and LB subjects and between children and adolescents. A total of 40 EB subjects, 40 LB subjects, and 30 sighted controls were recruited in two subgroups: children (6–12 years) and adolescents (13–19 years). Data were acquired using a 3T MR scanner. Analyses of blood oxygen level dependent (BOLD), functional connectivity (FC), correlation, and post hoc test for multiple comparisons were carried out. Difference in BOLD activity was observed in EB and LB groups in visual cortex during tactile perception, with increased FC of visual with dorsal attention and sensory motor networks in EB. EB adolescents exhibited increased connectivity with default mode and salience networks when compared with LB. Functional results correlated with duration of training, suggestive of better performance in EB. Alteration in sensory and visual networks in EB and LB correlated with duration of tactile training. Age of onset of blindness has an effect in cross-modal reorganization of visual cortex in EB and multimodal in LB in children and adolescents.

Keywords

tactile perception functional connectivity visual cortex fMRI early blind late blind sighted control

Tactile and spatial perception is a multisensory process for encoding and identifying egocentric and allocentric space in visually impaired people (Gori et al., 2017; Sathian, 2016). The visually impaired can be divided/grouped/categorized into early blind (EB, loss of vision within 8 months from birth) and late blind (LB, loss of vision with onset of 4 years from birth or more). Touch perception sensory system is better in blind people when compared with sighted (blindfolded) people (Sathian, 2016; Sathian & Stilla, 2010). Neuroimaging and functional magnetic resonance imaging (fMRI) studies using blood oxygen level dependent (BOLD) have reported stimulation of visual cortex while processing tactile stimuli (such as microspatial task and tactile discrimination) in EB and LB in comparison to sighted controls (SCs; Burton et al., 2004; Collignon et al., 2013; Sabbah et al., 2017; Sathian & Stilla, 2010; Stilla et al., 2008) and during tactile object and shape identification tasks in EB and LB (Jao et al., 2015; Hinkley et al., 2009).

Deprivation in a sensory modality leads to alterations in other sensory modalities, which may or may not cause changes in brain structure, function (neural interactions), and cognition processes (Lazzouni & Lepore, 2014). Connection between parietal and occipital cortical regions of brain in visually impaired individuals has been associated with utility of visual cortex for non-visual functions and cross-modal plasticity in corticocortical pathways (Amedi et al., 2010; Ptito et al., 2008; Qin et al., 2013; Voss, 2013).

Regional alterations of visual cortex differ depending on onset of blindness in EB and LB subjects (Jiang et al., 2017; Voss et al., 2016). LB individuals show varying experience with sensory deprivation, which is often ignored while making comparisons with the results of EB people (Voss, 2013). Studies on tactile perception (shape/geometry) have been reported cortical reorganization of visual cortex, without exploring the influence of plasticity on other networks of brain in EB, LB, and SC.

The objective of the study was to investigate perception of objects and shapes and its influence on cortical reorganization in EB and LB after vision loss during critical developmental time, which is lacking in literature. Correlation of critical development period, tactile training effect, and global cognition with hemodynamic response and functional connectivity (FC) during tactile processing was evaluated. We hypothesize that the effect of training will have an influence on FC in sensory and visual networks, and hence EB may reveal a higher BOLD response.

Materials and Methods

Subject Detail

Visually challenged subjects (n = 103) were screened in neuro-ophthalmology clinics of our institute after approval by Institute’s Ethical Committee. Visually impaired subjects were diagnosed in accordance with WHO criterion for blindness (visual acuity [VA] of better eye <20/400) (Vashist et al., 2017). VA tests were carried out using Snellen’s or log Minimum Angle of Resolution (MAR). If vision was less than 1/60, then finger counting was seen in well-lighted room for different distance range, that is, from 1 meter close to face, hand movement close to face, and finally light perception test done at 90 cm in dark room with indirect ophthalmoscope and projection of light in four quadrants. If patients were not able to perceive light, then for confirmation, a visual evoked response test (flash VER) was carried out. Torch light examination was done for ocular movements and pupillary reactions. Slit lamp examination was used to look for causative diagnosis such as anophthalmia, microphthalmos, cataract, sclerocornea, and so forth. Posterior segment examination was carried out for retinal evaluation for diagnosing conditions such as retinopathy of prematurity, retinitis pigmentosa, retinal detachment, chorioretinal coloboma, retinoblastoma, and other retinal disorders.

A total of 40 EBs (loss of sight at birth or before 8 months), 40 LBs (loss of sight after 4 years of age), and 30 sighted (with normal vision (6/6)) subjects (Table 1 and Table S1, S2, S3) were recruited. Age was matched for EB and LB and checked by comparing age means among children and adolescent’s groups, and no significant difference was observed. Subjects were explained about study, and informed consent form was signed by their family member or legally acceptable representative, prior to the study. Cutoff age in defining EBs varies across the studies ranging from a few months to 3 years, and therefore in this study, EBs were defined as loss of sight at birth or before 8 months and LBs were those who lost the eye sight after 4 years and older (Ungar, 2000) to avoid any overlap between two groups. Participants were examined for right-handed as per Edinburg handedness inventory (Oldfield, 1971). Cognitive assessment was done by using Mini-Mental State Examination (MMSE) and Montreal Cognitive Assessment (MoCA) rating scales (Reischies & Geiselmann, 1997; Wittich et al., 2010). MoCA BLIND rating scale excludes visuospatial/executive function component of MoCA scale.

Table 1.

Demographic Details (in Mean ± SD [Mode, Median] Wherever Applicable).

Details	Early blind	Late blind	Sighted control
Children group (6–12 years)
Sample size	n = 20	n = 20	n = 15
Gender	10 M/10 F	7 M/13 F	12 M/3 F
Age	9.45 ± 1.8 (8,9)	10.2 ± 2.1 (11,11)	10.1 ± 1.9 (11,11)
Onset age of blindness	2.5 ± 2.9 (0,1) months	4.5 ± 0.8 (4,4) years	NA
Duration of blindness (years)	9.2 ± 1.8 (8,9)	5.7 ± 2.6 (2,6)
Tactile training in months	36.25 ± 17.56 (24,34)	35.15 ± 19.36 (12,33.5)	92.0 ± 37.9 (108,120)
MoCA score	12.50 ± 5.06 (8,13)	14.6 ± 4.5 (8,16)	2 ± 1.5
MMSE score	11.25 ± 4.98 (15,11)	13.65 ± 4.6 (7,15)	1.1 ± 1.4
Adolescents group (13–19 years)
Sample size	n = 20	n = 20	n = 15
Gender	9 M/11 F	8 M/12 F	9 M/6 F
Age	14.4 ± 1.8 (15, 14.5)	15.3 ± 1.8 (14,14.5)	19.53 ± 2.99 (19,19)
Onset age of blindness	2.7 ± 3.2 (0.0) months	4.8 ± 1.5 (4,4) years	NA
Duration of blindness	14.19 ± 1.8 (12,14.05)	10.45 ± 2.32 (10,10)
Tactile training in months	112.75 ± 21.89 (108,08)	111.6 ± 21.36 (108,108)	202.4 ± 32.7 (204,204)
MoCA score	16.3 ± 5.56 (19,19)	17.75 ± 2.65 (16,17)	4.4 ± 0.9
MMSE score	15.05 ± 5.57 (20,17)	15.3 ± 1.8 (14,14.5)	5.0 ± 1.5

Note. MoCA = Montreal Cognitive Assessment; MMSE = Mini-Mental State Examination.

Inclusion and Exclusion Criteria

Right-handed educated school-going blind children and adolescents with better eye VA <20/400 (no visual perception) were enrolled into the study. Subjects with any other neurological/psychiatric disorder and any contraindication to MRI were excluded from study.

Data Acquisition

MR imaging were carried out in a 3 T MR scanner (Achieva 3.0 T TX, M/s. Philips Medical Systems) with a 32-channel head coil. BOLD imaging for tactile perception task was carried out by using echo planar imaging with repetition time (TR)/echo time (TE) = 2000/30 ms, no. of slices = 29, slice thickness = 4.5 mm, flip angle = 90°, slice gap = 0 mm, and number of dynamics were 160. Sagittal isotropic (1 mm) 3 D T1-weighted imaging was acquired using fast Fourier echo-based sequence with inversion time (TI) = 1100 ms, TR = 1900 ms, TE = 3.37 ms, and no. of slices = 180.

Task Details

Tactile perception task of object and shapes was acquired in one single fMRI session. To avoid imagery component, object and shapes were presented alternatively. Eight shapes and eight objects were presented over three blocks with defined onset and duration (Supplemental Figure S1). All sighted subjects were blindfolded during entire session of MRI. The tactile perception stimulation (active state) consisted of three-dimensional representation of everyday objects and regular geometrical shapes. All objects were non-magnetic, small items (radius/vortices = 2–3.5 cm) that could be identified tactually. Fourteen geometrical shapes (e.g., cube) fabricated from Perspex and 10 real-object representations (e.g., mango) made of wood and expanded polystyrene foam were presented (Figure S1). These items were standardized on 20 normal subjects and were able to identify them consistently (82%), with their eyes closed. Participants who underwent fMRI did not have prior knowledge of the objects presented to them.

A specially designed MR-compatible circular platform (Lucite material) positioned above abdomen of participant was used to present objects comfortably in supine position. Objects were mounted with the help of grove on the circular sheet (with eight equally spaced groves) and were presented at regular time interval (5 s) for each object. Subjects were instructed to explore object (using their right hand) and try to identify and recognize the representation based upon texture, depth, and shape of the object. Because we don’t have MR-compatible autochanger of objects, object and shapes were removed and changed manually (first author). The presence of eight grooves ensured perception of eight objects/shapes, and time window for changing objects, without any somatosensory stimulation. During baseline phase, subjects were instructed not to move their fingers/arm with their forearms comfortably resting on a Lucite circular platform positioned over their abdomen (Figure S1).

A block design with four alternating cycles of activity (perception task) and rest (that served as a baseline condition) was used. Task was generated using E-prime (version 1.1, Psychology Software Tools, Inc., USA) and presented to the instructor using MR-compatible 22″ display monitor (E-sys, M/s Philips Healthcare) for manual removal and replacement of each object and shape.

Data Processing

Image processing and statistical analyses were carried out using SPM12 (v4667) software (Achard & Bullmore, 2007) implemented in MATLAB (R2019a; The Math Works, Natick, MA, USA). Realigned (motion corrected) images were normalized with respect to Montreal Neurological Institute (MNI) template image (Mazziotta et al., 1995) and subsequently spatially smoothened using an isotropic Gaussian kernel (6 mm full-width-at-half maximum). BOLD activation patterns were estimated using Generalised Linear Model (GLM) by assigning regressor value. The regressor for each object and shape was defined by specific onset and duration of active and baseline block in a single trial, and confounds were resultant six translational and rotational parameters. Group analyses were done using two-sample t test (p(Family wise error (FWE)) < 0.05, extent threshold = 10 clusters) for intergroup (LB > SC; EB > LB with contrast: 1, –1) and analysis of variance (children [LB > SC; EB > LB with contrast: 1, –1] and adolescent group [LB > SC; EB > LB with contrast: 1, –1]) for main effects analysis between groups. The conjunction analysis (EB and LB with contrast defining F test and assigning contrast) was carried out for obtaining common activation in visually deprived groups (Friston et al., 1999). Brain coordinates were converted from MNI frame to Talairach frame using Ginger ALE software and brain areas estimated using TD client using Talairach and Tornoux atlas (Eickhoff et al., 2009, 2012; Lancaster et al., 1997, 2000; Talairach & Tournoux, 1988; Turkeltaub et al., 2002). In addition, intergroup comparisons were carried out using post hoc test (Bonferroni) (version 12, STATA). The network properties of each node were also investigated to demonstrate distribution of regions with significant differences between six groups at same threshold (p < .05). Finally, Spearman correlations between BOLD signal changes and duration of blindness and also with cognitive assessment data were calculated in blind and SC groups (p < .05 uncorrected).

Connectivity Analyses

Task-based FC analysis was carried out by using CONN toolbox version 18 C (Whitfield-Gabrieli & Nieto-Castanon, 2012). Data were preprocessed by using default pipeline for volume-based estimation that consists of functional realignment and unwarping, slice time correction, coregistration, and outlier identification for BOLD signal change by computing for each and every timepoint (Andersson et al., 2001; Henson et al., 1999). Structural and functional images were normalized to MNI template (Ashburner & Friston, 2005). Functional data were smoothened by using Gaussian Kernel of 6 mm full width half maximum to improve signal-to-noise ratio. Preprocessed data were then denoised for reduction of artifacts and residual movement effects by taking the confounding effect of paradigm and region of interest (ROI). First-level analysis was performed for estimation of seed-based connectivity and region-based connectivity for calculation of graph theory. ROI-level graph theory estimation was calculated by thresholding connected ROI-to-ROI correlation coefficient matrix (z > 0.5) (Achard & Bullmore, 2007; Latora & Marchiori, 2001). Second-level analysis was performed to evaluate group differences and testing of hypothesis based on population group inferences. Functional data were analysed using CONN FC toolbox in SPM12, using default parameters (Whitfield-Gabrieli & Nieto-Castanon, 2012). Seed-based correlation analysis was done for tactile perception by defining a seed to voxel ROI on primary visual cortex and somatosensory area.

Results

Cognitive Assessment

Spearman correlation coefficient was calculated for assessment of relationship between tactile training with MoCA and MMSE rating scale. There was a significant positive correlation at p = .01 (two tailed) between duration of tactile training and global cognition for children (EB1, LB1) and adolescents (EB2, LB2) groups (Table 2).

Table 2.

Correlation Analysis Between Tactile Training and Rating Scales (MoCA, MMSE) Across Visually Deprived Groups.

Rating scales	Statistics	EB1 (N = 20)	EB2 (N = 20)	LB1 (N = 20)	LB2 (N = 20)
MoCA	Pearson correlation (r)	0.937	0.977	0.991	0.749
MoCA	Sig. (2-tailed)	0.000	0.000	0.000	0.000
MMSE	Pearson correlation (r)	0.930	0.971	0.999	0.633
MMSE	Sig. (2-tailed)	0.000	0.000	0.000	0.003

Note. EB = early blind; LB = late blind; MoCA = Montreal Cognitive Assessment; MMSE = Mini-Mental State Examination.

BOLD

EB and LB subjects had no visual perception. Data of one EB subject were excluded due to a pathological diagnosis and another because of diffuse perception of light. On conjunction analysis, tactile perception evoked BOLD activity in ventral fusiform gyrus, bilateral Brodmann areas (BA) 6, 7, 18, 39, left sensorimotor cortices (BA 1, 2, 3, 5), and superior parietal lobule (BA 7) in all groups. EB, LB, and SC groups were further subdivided into children (6–12 years) and adolescent (13–19 years) groups for the evaluation of intergroup brain responses during tactile perception task (Figure 1).

Figure 1.

BOLD task-induced activations for early blind (A, B), late blind subjects (E, F) and sighted control (I, J) in the age range of 6–12 years and for early blind (C, D), late blind subjects (G, H) and sighted control subjects (K, L) in the age range of 13–19 years during tactile perception (shape [red] > object [yellow]), superimposed on a brain template.Note. Please refer to the online version of the article to view the figure in colour.

Sighted Control

In children group (SC1; 6–12 years), activation was observed in bilateral thalamus, right fusiform gyrus. Adolescent SCs (SC2) showed bilateral activation in Broca’s area (R > L), superior frontal gyrus, middle-medial frontal gyrus, precuneus middle temporal gyrus, left fusiform gyrus (BA 37), right superior temporal gyrus (L > R), hippocampus, and thalamus.

EB Subjects

In children group (EB1), bilateral BOLD activation in cuneus (BA 18), middle occipital gyrus, thalamus, and fusiform gyrus. EB adolescent group (EB2) revealed bilateral activations in middle temporal gyrus, visual cortex (BA 17, 18, 19; L > R), fusiform gyrus (BA 37) hippocampus and superior temporal gyrus (R > L).

LB Subjects

In children group (LB1), BOLD activation was increased in visual cortex area in V2 (BA 18), right lingual gyrus, and left fusiform gyrus. In LB adolescent group (LB2), BOLD response was observed in bilateral visual cortex (p < .05; R > L) involving visual cortex (BA 18, 19, 17), occipital fusiform gyrus, hippocampus, right cerebral middle and inferior temporal gyri, precuneus, and thalamus.

Intergroup Analysis

Intergroup analysis and multiple comparisons with post hoc test analysis with Bonferroni correction were estimated. Correlation with duration of tactile training and MoCA scores was evaluated (Figure 2, Table 3).

Figure 2.

Brain areas of BOLD activation with correlation duration of training and MoCA. Recruitment of visual cortex involving sensory stimulation during tactile perception is positively correlated with tactile training in (A) early blind and (B) late blind subjects. Correlation depicted between BOLD signal change (in visual cortex) and cognitive assessment (MoCA) in (C) early blind and (D) late blind.

Table 3.

Cluster Volume of Activation During Tactile Recognition in Controls, Early, and Late Blind Subjects Estimated Using One-Way ANOVA.

Region	BA	Hemisphere	Sighted subjects		Early blind		Late blind
Region	BA	Hemisphere	SC1	SC2	EB1	EB2	LB1	LB2
PocG	BA 1, 2, 3, 5	L	1,022	4,852	853	568	1,119	567
PocG	BA 1, 2, 3, 5	R	167	352	224	450	282	67
PrecG	BA 4	L	60	756	849	650	248	6
PrecG	BA 4	R	768	85	83	185	24	279
Medial frontal gyrus	BA 6	L	778	845	529	11	135	148
Medial frontal gyrus	BA 6	R	186	256	231	65	71	15
pSPG	BA 7	L	182	289	201	86	263	65
pSPG	BA 7	R	202	352	309	143	268	52
Cuneus, LOC	BA 18	L	26	125	352	956	237	964
Cuneus, LOC	BA 18	R	14	25	131	885	167	1,258
FG, MOG	BA 19	L	83	56	158	1,265	914	160
FG, MOG	BA 19	R	71	45	155	2,250	443	562
ITL	BA 37	L	15	9	83	96	38	269
ITL	BA 37	R	23	16	92	45	418	458
IPL	BA 39, 40	L	53	95	239	453	1,488	1,617
IPL	BA 39, 40	R	96	74	227	23	134	23
Cerebellum		L	309	385	1,707	175	143	969
Cerebellum		R	798	126	3,348	1,647	523	4,640

Note. PocG = postcentral gyrus; PrecG = precentral gyrus; pSPG = posterior superior parietal gyrus; LOC = lateral occipital cortex; FG = fusiform gyrus; MOG = middle occipital gyrus; ITL = inferior temporal lobule; IPL = inferior parietal lobule; BA = Brodmann area; EB = early blind; LB = late blind; SC = sighted control.

Children Age-Group

EB1 > SC1 (1–1)

EB group recruited bilateral occipital cortex (BA 18, 19) involving right lingual gyrus, hippocampus, left inferior occipital gyrus, and inferior temporal gyrus, in comparison with that in SCs. SC group revealed ipsilateral occipital fusiform gyrus and hippocampus with respect to EB group. On conjunction analysis, both the groups revealed left precentral and right fusiform gyrus activation.

LB1 > SC1 (1–1)

LB group evoked significant activation in bilateral middle and inferior occipital gyrus with respect to SC. Control group revealed contralateral activation in Broca’s and motor areas relative to LB. In conjunction analysis, only left precentral and post central gyrus activity is observed.

EB1 > LB1 (1–1)

EB group exhibited bilateral BOLD activation in V1, left middle temporal gyrus, hippocampus, and right fusiform gyrus in comparison to that in LB. In conjunction analysis, both groups showed activations in motor and right fusiform gyrus.

Adolescent Age-Group

EB2 > SC2 (1–1)

EB with respect to SCs showed activation in bilateral fusiform gyrus, cuneus, and thalamus. SCs when compared with EB group exhibited activation for tactile task in right thalamus, inferior frontal gyrus, and medial frontal gyrus. On conjunction analysis, left motor, somatosensory area, and right fusiform gyrus were seen.

LB2 > SC2 (1–1)

LBs exhibited BOLD activity in bilateral visual cortex (R > L), left cuneus, hippocampus, and right superior temporal gyrus. SCs revealed bilateral motor, somatosensory, and Broca’s areas in comparison with LB group. On conjunction analysis, hemodynamic response evoked activity in right fusiform, left motor, and inferior parietal lobule.

EB2 > LB2 (1–1)

Adolescent EB group when compared with LB group elicited strong BOLD activation in bilateral primary visual area (L > R). Left motor, left inferior occipital gyrus, inferior frontal gyrus, and right fusiform were present in both groups on conjunction analysis.

Correlation of Tactile Training With BOLD Data

EB and LB exhibited a positive correlation of tactile training with BOLD activations in inferior occipital, middle occipital, and lingual gyrus, on post hoc test for multiple comparison at p > .01 (Figure 3).

Figure 3.

Correlation plots depicting positive correlation between tactile training and BOLD response in early blind children groups (A) PCC, (B) LMOG, and (C) LFG; in adolescent early blind (D) LIOG, (E) LMOG, and (F) LSMA. In late blind children, a positive correlation was observed in the areas (G) RFG and (H) RMOG; in adolescents late blind group, the areas were (I) RLG and (J) RMTG at a significance level p > .01 (two-tailed tested for multiple comparisons).

Functional Connectivity

FC analysis was calculated by using sensory motor network and visual network as a seed ROI during tactile perception experimental condition for each group.

Sensory Network FC

Children Group

Increased FC of sensory network was observed with default mode areas, frontoparietal, and language area in LB. Decreased connectivity was observed with dorsal attention network during tactile perception of object and shapes LB when compared with that in SC (Figure 4A). SC group was showing sensory network connected with dorsal attention, frontoparietal, and salience network (Table S6). In EB group, increased connectivity of sensory network was observed with dorsal attention and salience network (Figure 4B, Table S6).

Figure 4.

Functional connectivity (graph theory) superimposed on the axial slice for sensory motor network during tactile perception in children group in (A) LB with respect to SC and (B) EB with respect to LB and in adolescent group in (C) LB with respect to SC and (D) EB with respect to LB, demonstrating significant positive connections (at pFDR corrected < 0.05) for seed level correction in ROI-to-ROI analysis.

Adolescent Group

Increased connectivity of sensory system with visual, dorsal attention, salience, and language network was present in LB when compared with SC (Figure 4C). In EB groups, a strong connectivity of sensory system was observed with dorsal attention, default mode, frontoparietal, salience, and visual network when compared with LB (Figure 4D, Table S4).

Visual Network FC

Children

FC of LB compared with SC revealed a strong connectivity of visual network with bilateral dorsal attention, default mode, left frontoparietal, and language network. Decreased FC was present with lateral prefrontal cortex in dorsal attention network (Figure 5A). EB group exhibited a strong connectivity of visual network among bilateral visual areas and with all other networks Dorsal Attention Network (DAN), Default Mode Network (DMN), Fronto-Parietal Network (FPN), Salience Network (SN) and Sensorimotor Network (SMN) (Figure 5B). However, some of the areas in DMN, FPN, Language Network (LN) and SN were showing decreased connectivity (Figure 5, Table S5).

Figure 5.

Functional connectivity graph theory superimposed on the axial slice for visual network during tactile perception in (A) LB with respect to SC children group, (B) LB with respect to SC adolescent group, (C) EB with respect to LB children group, and (D) EB with respect to LB adolescent group, demonstrating significant positive connections (at pFDR corrected < 0.05) for seed level correction in ROI-to-ROI analysis.

Adolescent Group

Increased connectivity of visual network with other networks of brain was observed in both EB and LB subjects during tactile perception of object and shapes (Figure 5C, 5D, Table S5).

Shape Versus Object

FC difference between object and shape perception were also estimated.

Children Group

Increased connectivity between paracingulate with cerebellum and interconnectivity of salience network was observed in LB children when compared with SC (Figure 6A). Increased connectivity in salience network (interconnected and with cerebellum areas) in EB children with respect to LB (Figure 6B, Table S6) was also noted.

Figure 6.

Functional connectivity graph theory for shape with respect to object in (A) for the contrast LB> SC children group, (B) EB > LB children group, (C) for the contrast LB> SC adolescents group, and (D) EB > LB adolescents group during tactile perception.

Adolescents Group

LB presented increased connectivity strength of salience network with default mode, frontoparietal, language in left hemisphere, and enhanced interconnectivity of salience network (Figure 6C). Increased connectivity was detected between dorsal attention and visual medial and decreased in salience network in EB when compared with LB (Figure 6D, Table S7). LB and SCs were not showing any significant difference for the involvement of visual network, and EB group is showing the clear involvement of visual network for the tactile perception processing (at pFDR> 0.05).

Tactile Perception Network in SC

Connectivity was increased in sensory, dorsal attention, frontoparietal, and salience network in children (Figure 7A). In adolescents group, increased connectivity of dorsal attention was observed with frontoparietal, sensory networks, and visual medial with visual lateral (Figure 7B, Table S8). The inference of this is that the SC group was not including the visual network in children group but the network is involved in adolescents group.

Figure 7.

Functional connectivity (graph theory) for (A) sighted children group and (B) adolescents group for shape > object contrast during tactile perception (at pFDR corrected ≪0.05) at seed level.

Discussion

Hemodynamic signal alteration and task-based FC between EB and LBs revealed differential occipital activation, suggesting brain plasticity mechanism associated with sensory experience during different stages and onset of blindness. Cortical and subcortical pathways relay across the brain for potential mechanism to counterbalance the loss of vision through other sensory modalities.

BOLD conjunction analysis revealed response in motor and visual cortex in both EB and LB groups. Bilateral activation of BA 18, 19, and 17 was observed in EB2 and LB2 subjects. EB1 recruited contralateral, while LB1 invoked ipsilateral visual cortex. EB group exhibit increased positive correlation between left parieto-occipital areas involving dorsal attention network and visual areas in EB but increased correlation of parieto-occipital network with right visual cortex. Alteration in hemodynamic response is associated with the neural reorganization in the parieto-occipital areas and sensory motor areas for encoding of tactile information processing of object and shapes (Leo et al., 2012).

Our results revealed reduced visual area recruitment in children than adolescent group and region-speciﬁc (primary visual cortex) cross-modal plasticity in LBs and EBs during critical developmental period (Buchel, 1998). In LB group, age of onset of blindness and duration of tactile experience affect reorganization of occipital area for tactile perception processing (Voss, 2013).

Secondary visual cortical areas were not responding in SCs involving fusiform gyrus, which may be associated with less effort to perceive objects. Occipital fusiform gyrus involvement may be attributed to the stereoscopic perception required during visualization of perceived objects (Collignon et al., 2013).

Hemodynamic response in bilateral inferior occipital gyrus in EB (children and adolescent groups) as well as LB adolescents is in concurrence with an earlier report and may be ascribed to object perception through tactile processing (Jiang et al., 2017; Kravitz et al., 2013; Voss, 2013). The occipital fusiform gyrus and thalamus recruitment in LBs may be attributed to visual imagery processes associated with earlier visual experience and in SCs for object perception (Bauer et al., 2017; Renier et al., 2010). Furthermore, LB and SC groups may have used their (previous) visual experience to solve the task, suggestive of residual visual imagery capabilities affecting cross-modal plasticity (Collignon et al., 2013; Jao et al., 2015).

Non-visual recruitment of visual cortex has been reported to compensate for functional specialization of other sensory perception (e.g., touch auditory) (Corbetta & Shulman, 2002; Klinge et al., 2010). This suggests that a specific brain area is allocated for cognitive process in visual domain in case of early visual deficit. In adolescent group of EB and LB, an intact connectivity and hemodynamic response in visual areas (V1, V2, V3, V4, V5, and V6) in inferior, middle, and superior temporal cortex and inferior parietal lobule areas were observed. The processing of visual information requires both ventral and dorsal visual pathways (Qin et al., 2013; Wen et al., 2018). Tactile perception task-based activations in adolescent group suggest alterations in these pathways for processing tactile and spatial information without visual perception. Functional relevance of right dorsal stream was observed during spatial processing of objects in EB1, but not in LB1.

Intact FC of motor, somatosensory area with occipital cortex in adolescent group of blinds in comparison to children group suggest that V3d-V3A and V5 areas subserve visuospatial and kinaesthetic processing in blind groups and SCs (Amedi et al., 2010; Jao et al., 2015; Sathian, 2016). Positive correlation between duration of training and hemodynamic signal variability suggests that blindness leads to speciﬁc cross-modal reorganization in right dorsal stream in concurrence with reports of early structural and functional modification of visual cortex (Lazzouni & Lepore, 2014). Critical developmental period affects cross-modal reorganization of V1 and associated areas in LB1. Processing of various sensory-based non-visual processes suggests an altered reorganization of occipital area in EB and LB.

The neurophysiology aspect of the visual and tactile perception is based on object characteristics, orientation, and attention. Top-down attention signals and bottom-up tactile inputs interact for processing targeted stimulus as seen in V1 area for somatosensory processing of tactile stimulus for haptic object identification (Sathian, 2016). Differences were observed in dorsal and ventral extension till V5 in EB and LB that may be associated with complex perceptual task (effort making in approaching towards objects). Although cross-modal alteration exists in occipital region of both EB and LBs, pattern of reorganization is different in children and adolescents. EB and LB showed functional alteration in right dorsal stream network between adolescent and children groups during tactile-based perception of objects. Dorsal stream’s capacity to compute spatial intricacies is correlated with non-visual stimulus during early developmental period (Hou et al., 2017; Leo et al., 2012).

The improvement of psychological space selectivity in visual cortex is driven by inherent connectivity of different areas that are associated with processing of this area with a network of different area that is associated for processing of this tactile perception and visual perception (Hasson & Frith, 2016; Kravitz et al., 2013; Mahon & Caramazza, 2011). During tactile perception, processing of objects and shapes undergo visuospatial attention, and EBs demonstrate an alteration in interaction between right dorsal visual cortex to intra parietal lobule when compared with LBs (Sabbah et al., 2017). Hence, differences in FC of dorsal stream between EB and LBs may be attributed to alterations in coding and decoding tactile processing.

Decreased FC from bilateral primary visual cortex to cuneus, lingual gyrus involving BA 18 and 19 in LB children indicates a detachment in ocular system (Knudsen, 2004; Wen et al., 2018). Direct corticocortical association between primary somatosensory cortex and visual cortex in EB (both EB1 and EB2) suggests early age deprivation may lead to involvement of visual cortex in other sensory phenomenon (Klinge et al., 2010; Ptito et al., 2008; Qin et al., 2013). In LB2, visual cortex reorganization was associated after visual information processing, but EB was much better trained for processing of tactile perception in visual cortex. Hence, there may be a difference in reconfiguration of visual cortex of EB and LB associated with altered FC among visual cortex to somatosensory area in both groups. Thus, it may be speculated that visual deficit following a vital developmental stage induces modification in top-down signalling, mental imagery network, and visuospatial attention networks for tactile perception processing by multisensory conjunction regions (Corbetta & Shulman, 2002; Kosslyn & Thompson, 2003; Macaluso et al., 2005).

This study suggests that the EB subjects have better integration of visual network with other sensory networks when compared with the LB. Visual, salience, and object recognition network areas showed a relationship with tactile training in EB group than LB group also in adolescent group than children group. EB and LB subjects following age of onset and tactile training duration affects sensory and visual networks differently during tactile perception.

Limitation

Although study includes a reasonable sample size, SCs (especially in adolescent group) could not be age matched, as it was difficult to recruit willing adolescents.

Conclusion

EB exhibits better perception during non-visual task when compared with LB. Higher BOLD response and increased FC of visual cortex correlated with better performance. Early visual impairment and longer exposure (to tactile training) lead to an improvement in functional sensorial outcome while processing of non-visual stimulation by cross-modal reorganization in EB and multimodal reorganization in LB. Better understanding of visual cortex plasticity (cross-modal and multi-modal) will help in social readaptation by expanding other (intact) sensory networks.

Supplemental Material

sj-pdf-1-pec-10.1177_0301006621991953 - Supplemental material for Visual Cortex Alterations in Early and Late Blind Subjects During Tactile Perception

Supplemental material, sj-pdf-1-pec-10.1177_0301006621991953 for Visual Cortex Alterations in Early and Late Blind Subjects During Tactile Perception by A. Ankeeta, S. Senthil Kumaran, Rohit Saxena, Sada N. Dwivedi and Naranamangalam R. Jagannathan in Perception

Footnotes

Acknowledgements

National School for Blind provided invaluable assistance, advice, and subject recruitment throughout this project.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Department of Science and technology (CSI), New Delhi, India (vide grants SR/CSI/23/2009 and SR/CSI/176/2012). N. R. J. thanks SERB, DST for the ward of J C Bose Fellowship.

ORCID iD

S. Senthil Kumaran

Supplemental Material

Supplemental material for this article is available online.

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