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Neuropsychologia 68 (2015) 5970

Contents lists available at ScienceDirect

Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Spatial imagery relies on a sensory independent, though sensory


sensitive, functional organization within the parietal cortex: A fMRI study
of angle discrimination in sighted and congenitally blind individuals
Daniela Bonino a, Emiliano Ricciardi a,b,n, Giulio Bernardi a, Lorenzo Sani a, Claudio Gentili c,
Tomaso Vecchi d,e, Pietro Pietrini a,c
a
Laboratory of Clinical Biochemistry and Molecular Biology, Department of Surgery, Medical, Molecular Pathology, and Critical Care,
University of Pisa, Pisa, Italy
b
MRI Lab, Fondazione G. Monasterio Regione Toscana/C.N.R., Pisa, Italy
c
Clinical Psychology Branch, Department of Surgery, Medical, Molecular Pathology, and Critical Care, University of Pisa, Pisa, Italy
d
Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy
e
Brain Connectivity Center, National Neurological Institute C. Mondino, Pavia, Italy

art ic l e i nf o a b s t r a c t

Article history: Although vision offers distinctive information to space representation, individuals who lack vision since
Received 23 August 2014 birth often show perceptual and representational skills comparable to those found in sighted individuals.
Received in revised form However, congenitally blind individuals may result in impaired spatial analysis, when engaging in visual
31 December 2014
spatial features (e.g., perspective or angle representation) or complex spatial mental abilities. In the
Accepted 5 January 2015
present study, we measured behavioral and brain responses using functional magnetic resonance ima-
Available online 6 January 2015
ging in sighted and congenitally blind individuals during spatial imagery based on a modied version of
Keywords: the mental clock task (e.g., angle discrimination) and a simple recognition control condition, as conveyed
Supramodality across distinct sensory modalities: visual (sighted individuals only), tactile and auditory. Blind in-
Spatial representation
dividuals were signicantly less accurate during the auditory task, but comparable-to-sighted during the
Blindness
tactile task. As expected, both groups showed common neural activations in intraparietal and superior
Parietal cortex
Sensory-deprivation parietal regions across visual and non-visual spatial perception and imagery conditions, indicating the
more abstract, sensory independent functional organization of these cortical areas, a property that we
named supramodality. At the same time, however, comparisons in brain responses and functional con-
nectivity patterns across experimental conditions demonstrated also a functional lateralization, in a way
that correlated with the distinct behavioral performance in blind and sighted individuals. Specically,
blind individuals relied more on right parietal regions, mainly in the tactile and less in the auditory
spatial processing. In sighted, spatial representation across modalities relied more on left parietal re-
gions. In conclusions, intraparietal and superior parietal regions subserve supramodal spatial re-
presentations in sighted and congenitally blind individuals. Differences in their recruitment across non-
visual spatial processing in sighted and blind individuals may be related to distinctive behavioral per-
formance and/or mental strategies adopted when they deal with the same spatial representation as
conveyed through different sensory modalities.
& 2015 Elsevier Ltd. All rights reserved.

1. Introduction vision in shaping and modulating these functions, as well as in


inuencing the development of the neural structures underlying
Since the pivotal studies by Kosslyn in the seventies (e.g., these abilities, however, remains still to be fully dened.
Kosslyn, 1973), there is ample evidence that chronometric prop- Although vision offers distinctive information for the re-
erties of mental images are shared with visual percepts. The role of presentation of the surroundings, so that for a long time it has
been thought to be crucial for the development of spatial abilities,
a growing body of evidence suggests that the lack of visual
n
Correspondence to: Laboratory of Clinical Biochemistry and Molecular Biology, experience may have just limited effects on the perception
University of Pisa, Azienda Ospedaliero Universitaria Pisana, Santa Chiara, Via
Roma, 67 Bldg. 43, I-56127 Pisa, Italy. Fax: 39 050 993556. and mental representation of space (Cattaneo et al., 2008;
E-mail address: emiliano.ricciardi@bioclinica.unipi.it (E. Ricciardi). Ricciardi et al., 2010). As a matter of fact, individuals who are

http://dx.doi.org/10.1016/j.neuropsychologia.2015.01.004
0028-3932/& 2015 Elsevier Ltd. All rights reserved.
60 D. Bonino et al. / Neuropsychologia 68 (2015) 5970

visually-deprived since birth show similar levels of performance to angle size detection relies on a bilateral, though left-dominant,
sighted individuals in distinct spatial discrimination tasks, in- recruitment of posterior parietal regions (Formisano et al., 2002;
cluding navigation, number processing or action planning (Aleman Trojano et al., 2000). Further, at a behavioral level, congenitally
et al., 2001; Cattaneo and Vecchi, 2011; Fleming et al., 2006; blind individuals showed signicantly lower degrees of perfor-
Ricciardi et al., 2010; Vecchi, 1998). mance in a spatial-imagery task of angle discrimination as com-
Neuropsychological, lesion and functional brain studies in- pared to sighted ones (Noordzij et al., 2007).
dicate that spatial perceptual abilities and spatial mental re- Based on the observations discussed above, we predicted that
presentations critically rely on posterior parietal regions (Ricciardi spatial imagery would be associated with a shared supramodal
et al., 2010; Sack et al., 2002a, 2002b; Trojano et al., 2002, 2000). functional response within the parietal cortical areas related to
Interestingly, these cortical regions are activated during both spatial perception, that is, this area would be recruited in-
perceptual and imagery tasks, regardless of the sensory modality dependently from visual experience and from the sensory channel
through which such a spatial information has been acquired used for angle spatial perception. At the same time, given the
(Cattaneo et al., 2008; Ptito et al., 2011; Ricciardi et al., 2014a, distinctive features of mental processing, as well as previous
2014b, 2010; Ricciardi and Pietrini, 2011). Furthermore, con- ndings from distinct studies on spatial perception in sighted and
genitally blind individuals recruit intraparietal and superior par- congenitally blind individuals obtained in our own lab (Bonino
ietal regions during non-visual spatial processing and localization et al., 2008; Ricciardi et al., 2006, 2007), we also expected that
(Weeks et al., 2000), spatial imagery (Vanlierde et al., 2003), or- within this common supramodal functional architecture, patterns
ientation discrimination (Ptito, 2005), spatial attention and of neural response would be shaped to some extent by visual ex-
memory (Bonino et al., 2008), and even numerical comparison perience and by the distinctive features of the specic sensory
(Szucs and Csepe, 2005) tasks. Altogether, these observations modality utilized to acquire spatial information.
strongly suggest a more abstract, visual-independent sensory re-
presentation of spatial information in the human brain, that is, a
supramodal functional organization. 2. Materials and methods
On the other hand, blind individuals do acquire a reduced
amount of sensorial information, in terms of both classical visual 2.1. Subjects
spatial features (e.g., perspective or angle representation) and
their simultaneous and integrated perception, as compared to We measured neural activity in 10 sighted (7M/3F, mean
sighted ones (Cattaneo and Vecchi, 2008). At a behavioral level, age7s.d. 29 73 years) and nine congenitally blind (5M/4F,
these perceptual limitations result in impaired responses when 43716 years; age group comparison, t-test Bonferroni corrected,
individuals perform spatial imagery tasks that rely on visually- p n.s.) right-handed healthy volunteers. Eight subjects were blind
based representations, or that involve complex spatial mental from birth, and one became totally blind by the age of 18 months
abilities (Cattaneo et al., 2008; Gori et al., 2014; Struiksma et al., (she lost the right eye vision at 10 months, and the left eye vision
2009). For instance, performance differed between congenitally at 18 months) and had no recollection of any visual memory. Only
blind and sighted participants in a spatial-imagery task of angle individuals with a peripheral cause of congenital blindness were
discrimination, but not in a visually-based or auditory-based admitted to the study. In order to avoid any possible bias due to
imagery tasks of object form (Noordzij et al., 2007). Similarly, the familiarity with the task (e.g. Noordzij et al., 2007), we selected
dealing with multiple or three-dimensional spatial mental re- only sighted and congenitally blind volunteers who had experi-
presentations may be rather problematic for congenitally blind ence of analogical or traditional tactile Braille clocks, respectively.
individuals (Vecchi, 1998; Vecchi et al., 1995). Indeed, blind in- Due to signicant head movement artifacts (greater than one voxel
dividuals develop their cognitive mechanisms through touch and sixe), three congenitally blind individuals had to be dismissed, so
hearing, which only allow for a sequential processing of informa- that data from six congenitally blind (4M/2F, 39 716 years; age
tion. This may force people who lack vision since birth to rely, at a group comparison, Bonferroni corrected p n.s.) volunteers en-
higher cognitive level, on partially different non-visual spatial tered the behavioral and brain functional data analysis. Causes of
processes (Noordzij et al., 2007; Vecchi, 1998). blindness for each of the six individuals are reported in Table 1.
At a neural level, brain responses across distinct perceptual All sighted and blind participants received a clinical examina-
tasks in sighted and congenitally blind individuals show both si- tion, including routine blood tests and a brain structural MRI scan,
milar patterns of activation within wide portions of association to exclude any disorder that could affect brain function or meta-
cortical areas (Ricciardi et al., 2014a) and a differential recruitment bolism, other than blindness in the blind group. No subject was
of primary visual cortical areas (Vanlierde et al., 2003), due to
taking any psychotropic medication. All participants gave their
cross-modal plastic functional rearrangements in vision-related
written informed consent after the study procedures and potential
cortical areas (Kupers et al., 2011a; Ricciardi and Pietrini, 2011).
risks had been explained. The study was conducted under a pro-
Overall, these ndings indicate that in the brain supramodal and
tocol approved by the Ethical Committee at the University of Pisa
cross-modal functional organizations coexist. As a matter of fact,
we can think of the two phenomena as of the two sides of the
same coin: supramodality is the functional architecture that takes
Table 1
place despite the lack of visual input, whereas cross-modal plasti- Characteristics of the congenitally blind volunteers enrolled in the study.
city is the functional rearrangement that occurs because of the lack
of sight (Ricciardi et al., 2014a, 2014b). Gender Age Age of blindness onset Cause of blindness
In the present study, we wished to examine to what extent (the (years) (months)
lack of) visual experience and the specic features of the distinct
Male 31 0 Congenital glaucoma
sensory modalities may affect the brain functional architecture Male 58 0 Congenital glaucoma
that sustains spatial imagery. Specically, we measured brain re- Male 53 0 Congenital optic atrophy of
sponses in both sighted and congenitally blind individuals during unknown cause
an angle discrimination task in which stimuli were presented Female 42 0 Retinopathy of prematurity
Female 20 18 Congenital glaucoma
through the visual (sighted subjects only), tactile and auditory Male 57 0 Congenital cataract
pathways. Previous studies showed that in sighted individuals
D. Bonino et al. / Neuropsychologia 68 (2015) 5970 61

two analogical clocks for 2 s, with a 1 s-long inter-stimulus period.


Stimulation periods in the tactile and visual experimental tasks
were established by performing behavioral pre-test measures in
independent samples of individuals. Across all the three experi-
mental conditions, inter-trial interval (ITI) lasted 5 s, during which
the participants provided their responses. Within each fMRI ses-
sion, participants were presented with 18 trials.

2.2.2. Control conditions


Two control tasks for the tactile and auditory conditions were
administered to control for the sensorimotor and the semantic
components of the MCT.
For the tactile control task, non-sense scrambled wooden-
made clocks were used. The scrambled clocks were identical in
shape and dimension (clock diameter: 20 cm, long hand: 8 cm,
short hand: 5 cm) to the analogical clocks, but the two wooden-
made hands were positioned so that they did not form any angle.
The tactile control task followed the same presentation timing of
the tactile MCT. In a simple discrimination task, participants were
instructed to tactilely discriminate whether both the clocks of the
presented pair were analogical clocks or whether one of them was
a scrambled one. During each tactile control run, 28 scrambled
clocks and only four analogical clocks were administered.
Control auditory stimuli had the same characteristics of those
presented during the auditory MCT, but a time, rather than an
angle, discrimination task was performed. Participants sequen-
tially listened to two clock times for 2 s each, with a 1 s-long inter-
stimulus period, and had to decide which of the two clock times
was the earliest one in a chronological order. In both control tasks,
participants provided their responses via foot pedals. The response
correspondence of right and left foot was randomized across
subjects, in order to control for any potential foot movement la-
teralization effect on brain activation. Across the two control
Fig. 1. Behavioral results. (A) fMRI design of the experimental tasks for the dif- conditions, ITI lasted 5 s, during which participants could provide
ferent sensory modality. ISI: inter-stimulus interval; ITI: inter-trial interval
their responses. Within each fMRI session, participants were pre-
(B) Accuracies in performance for the blind (red) and sighted (blue) groups during
the MCT conditions are shown in a graph bar plot. Signicant differences and in- sented with 18 trials.
teractions in the group and post-hoc analyses are reported in black/thick lines and As previous MCT studies had shown that in sighted individuals
gray/dotted lines for the repeated-measure ANOVAs between sighted and blind visual-based angle size detection relies on a bilateral, though left-
groups and for within sighted participants, respectively. Chance level is shown at dominant, recruitment of posterior parietal regions, we chose not
50% as a bold white line. (For interpretation of the references to color in this gure
legend, the reader is referred to the web version of this article.)
to perform any visual control task in order to limit overall scan-
ning time (Sack et al., 2002b; Trojano et al., 2002, 2000). All the
verbal stimuli used during auditory experimental conditions were
Medical School. All participants retained the right to withdraw administered by a MR-compatible pneumatic headphone system
from the study at any moment. (PureSound Audio System Wardray Premise Ltd. United Kingdom).
Visual stimuli were presented onto a rear projection screen viewed
2.2. Experimental tasks and stimuli by volunteers through the head coil prismatic mirror (visual eld:
25 wide and 20 high). Tactile stimuli were sequentially leaned by
2.2.1. Mental clock test an operator inside the MRI scanner on a magnetic compatible
A revised version of Paivios Mental Clock Test (Paivio, 1978; small table placed over the participant abdomen, to be sure that
MCT) was used in our fMRI protocol (Fig. 1A). Participants were each volunteer could effectively touch the stimuli without any
asked to mentally compare the convex angles formed by the hands head movement, as in similar tactile discrimination paradigms
of two analogical clocks, after they either perceived or imagined in adopted in previous experimental settings (Pietrini et al., 2004;
a sequential order a pair of clock faces prompted aurally, tactilely Ricciardi et al., 2007).
or visually (only for the sighted individuals). Participants had to Prior to the fMRI scanning exam, all volunteers performed a
decide in which clock the hands formed the wider convex angle 30 min long training session. Participants repeated the task across
and answered by pressing foot pedals. The response correspon- all the three sensory modalities, and the two control tasks, until
dence of right and left foot with the rst or second clock was they became familiar with the experimental paradigm. None of the
randomized across subjects, in order to control for any potential experimental stimulus pairs used during the training sessions was
effects of foot movements on brain activation. During the auditory employed in the subsequent fMRI experiment and no feedback
version of the MCT, volunteers sequentially listened to two clock was provided to the subjects.
times for 2 s each, with a 1 s-long inter-stimulus period. During
the tactile version of the MCT, participants were asked to se- 2.3. Image acquisition
quentially explore with both hands two wooden-made analogical
clocks (clock diameter: 20 cm, long hand: 8 cm, short hand: 5 cm) fMRI images were acquired using a Gradient Echo echoplanar
for 4.5 s each, with a 1 s-long inter-stimulus period. During the (GRE-EPI) sequence with a GE Signa 1.5 T scanner (General Electric,
visual version of the MCT, sighted participants sequentially viewed Milwaukee, WI). A scan cycle (repetition time (TR) 2500 ms) was
62 D. Bonino et al. / Neuropsychologia 68 (2015) 5970

composed of 21 contiguous axial slices (5 mm thickness, eld of regression analysis. The six movement parameters derived from
view (FOV) 24 cm, echo time (TE) 40 ms, ip angle 90, image the volume registration and the polynomial regressors to account
in plane resolution 64  64 pixels) and voxels dimensions were for baseline shifts and linear/quadratic drifts in each scan series
3.75  3.75  5 mm3. We acquired 10 (congenitally blinds) and 13 were included in the multiple regression analysis as regressors of
(sighted subjects) runs for each participant. In both groups, ac- no interest. Beta weights for the regressors that modeled the mean
cording to the specic experimental protocols, we recorded ve responses to each experimental condition were used as estimates
sessions of 126 brain volumes (e.g., tactile MCT and control tasks, of the strength of response relative to rest in each voxels. Beta
overall acquisition time 315 s), and ve sessions with 90 brain weights and T statistics for each experimental conditions were
volumes (e.g., auditory MCT and control tasks, overall acquisition transformed into the Talairach and Tournoux Atlas (Talairach and
time 230 s). Only sighted volunteers had three extra sessions with Tournoux, 1988) coordinate system, and resampled into 1 mm3
90 brain volumes (e.g., visual MCT, overall acquisition time 230 s). voxels for group analyses. Activations were anatomically localized
Each time series included 18 trial repetitions, began and ended on the sighted and congenitally blind group-averaged Talairach-
with 30 s and 20 s of no stimuli, respectively. transformed T1-weighted images, and visualized using normalized
High-resolution T1-weighted spoiled gradient recall (SPGR- SUMA (SUrface MApping with AFNI) surface templates.
TE 5.22 ms, TR 12.1 ms, FOV 240 mm with 256  256 acquisi- Group level analyses focused on, rst, identifying brain re-
tion matrix, 0.94  0.94 mm2 in-plane resolution, 120 axial slices sponses for each experimental condition in the two groups. Sec-
of 1.2 mm-thickness) images were obtained for each subject to ond, overlapping, supramodal and MCT-specic responses in both
provide a detailed brain anatomy during structural image sighted and congenitally blind individuals were characterized. Fi-
acquisition. nally, differential recruitments between sighted and congenitally
blind individuals were addressed, also through a comparison
2.4. Data analysis among indices of functional connectivity strength from seed re-
gions showing supramodal responses.
2.4.1. Behavioral data
During the fMRI sessions, accuracy for each experimental 2.4.2.1. Within-group and within-condition activations. A mixed-
condition was recorded. Individual average accuracies for the effect meta-analysis (3dMEMA) identied patterns of activation
distinct experimental MCT conditions were used in a repeated- within experimental conditions for each group. Specically, a
measure, three-way ANOVA to evaluate differences in accuracy within condition mixed-effects meta-analysis is equivalent to a
within- and between-experimental groups (sighted and con- one-sample T-test. Compared to a conventional T-contrast, the
genitally blind individuals) and sensory modalities (auditory and mixed-effects meta-analysis takes into account within-subject
tactile). Individual ages for the two groups were introduced as variability of response in an activated brain region and assigns
covariate. Post-hoc T comparisons were assessed for signicant each subject's contribution (from the individual T statistics of each
(p o0.05) effects or interactions. In sighted individuals only, a re- stimulus timeseries regression model) to the nal result based on
peated-measure, two-way ANOVA was used to assess differences a weighted instead of an equal treatment (Chen et al., 2012). The
across sensory modalities for the MCT condition. Statistical ana- correction of these second-level analyses across task-activated
lyses were performed by using IBMs SPSSs Statistics 21. regions was made by using Monte-Carlo simulations, run via
3dClustSim with a voxelwise threshold of 0.01 that resulted in a
2.4.2. fMRI data minimum cluster volume 4882 L, nearest-neighbor, for a cor-
The AFNI and SUMA software package was used to analyze and rected p value o0.05 at cluster level.
display functional imaging data (http://afni.nimh.nih.gov/afni,
(Cox, 1996)). Prior to standard preprocessing, the rst four vo- 2.4.2.2. Overlapping activations across conditions and across experi-
lumes and the last volume acquired were discarded (resulting in a mental groups. To identify cortical areas responding within-single
total of 85 volumes for the visual and auditory sessions, and 121 subject to auditory and tactile MCT in congenitally blind in-
for the tactile sessions) to allow the MR signal to remain at the dividuals and to auditory, visual and tactile MCT in the sighted
steady state. All raw volumes from the different runs were con- group, a modied conjunction analysis also was used (as detailed
catenated and coregistered (3dvolreg), temporally aligned in Beauchamp et al., 2008). Briey, the T-statistic of the contrast
(3dTshift), and spatially smoothed (isotropic Gaussian lter, between stimulation vs. rest was calculated independently for
FWHM 8 mm). Individual runs were normalized by calculating each experimental condition in each subject. Only signicant
the mean intensity baseline value for each voxel during the initial voxels showing a positive BOLD response to each sensory modality
(seven) and nal (three) resting volumes, and by dividing each were selected (threshold for the unisensory response was set at
voxel value by its mean intensity to estimate the percent signal uncorrected po 0.05) and combined using a logical AND. All voxels
change at each time point. Statistical analysis was performed using passing this test (signicant in Z7 sighted, or Z 5 early blind
a multiple regression to identify brain regions signicantly in- individuals) were classied as common across conditions (Fig. 2A).
volved in the auditory, tactile and visual MCT, and in the auditory A conjunction analysis was also used to create the mixed-ef-
and tactile control conditions. The mean response to each stimulus fects group map. A logical AND was performed with the mixed-
of each experimental condition was modeled with a separate re- effect meta-analysis identied patterns of activation within ex-
gressor, obtained by convolution of the task with a standard he- perimental condition at a corrected p o0.05 cluster-level, as de-
modynamic response model (BLOCK basis function), to shape the tailed for the within-group and within-condition responses
response to each of the 5 s (auditory and visual tasks) or 10 s (Fig. 2B). As supramodal areas, differentially from those cortical
(tactile tasks) periods of stimulus presentation and processing, regions showing a cross-modal plastic response, are present both
followed by the 5 s response periods. By modeling each type of in sighted and blind individuals, a logical AND also was used to
stimulus presentation, this resulted in ve regressors of interest overlap patterns of activation across experimental conditions be-
for the sighted subjects (auditory, tactile and visual MCT and aural tween experimental groups (Fig. 2B).
and tactile control tasks) and in four regressors of interest for the
blind subjects (auditory and tactile MCT and aural and tactile 2.4.2.3. Supramodal brain responses: correlation with behavioral
control tasks). Individual timepoints relative to uncorrected re- performances. According to the denition itself of supramodality,
sponses were censored, and thus not included in the multiple cortical areas showing a supramodal response to spatial
D. Bonino et al. / Neuropsychologia 68 (2015) 5970 63

Fig. 2. Overlapping activations across experimental conditions. Statistical maps showing overlapping activations across conditions in sighted and congenitally blind in-
dividuals as a result of single subject (A) and group (B) conjunction maps. The spatially-normalized results are projected onto single-subject hemisphere templates in
Talairach space for the two experimental groups in a lateral view.

discrimination (i.e., angle representation) task should show pat- correction (SVC), we created a binary mask across the four within
terns of neural activity that overlap between the sighted and the condition patterns of activation (at a whole brain corrected
blind groups. Furthermore, these areas should show higher task- po 0.05) for each group, used this volume as an inclusive mask
specic neural responses across the MCTs as compared to the and calculated via 3dClustSim the minimum cluster size for the
control conditions, and neural activity should correlate with the sighted and blind groups for a SVC corrected po 0.05 with a voxel-
behavioral performances across sensory modalities. wise threshold of 0.025 (nearest-neighbor, minimum cluster size
First, as a repeated-measure two-way ANOVA-comparable to of 844 L for sighted, and of 702 L for congenitally blind
behavioral outcomes-could not be performed on functional data subjects).
due to unbalanced samples (as reported in Section 2, data from In order to characterize further the differential access to su-
three blind subjects had to be discarded due to excessive head pramodal areas between experimental conditions and groups, a
motion artifacts), a mixed-effect meta-analysis was used to iden- mixed-effect meta-analysis was used to identify parietal clusters
tify only those brain areas with a within-group stronger response with a within-group stronger response to tactile or auditory MCT as
to both tactile and auditory MCT as compared to the control compared to the control conditions (one-sample T contrasts as
conditions. In details, beta weights and T statistics of the differ- above, but separated for the auditory and tactile modalities; volumes
ences between MCT and control conditions were considered for of interest limited to the mixed-effects group conjunction maps
the two sensory modalities (i.e., auditory and tactile) in a single across experimental conditions and groups; voxel-wise threshold of
one-sample T contrast (Fig. 3A). To perform a small volume 0.05 and an arbitrary minimum cluster size of 200 L Fig. 3B).

Fig. 3. Comparison between experimental conditions and performance/brain response correlation. Statistical maps showing brain regions with a signicantly different
response between MCT and control conditions across- (A) and within- (B) sensory modalities in sighted and congenitally blind individuals. (C) Clusters showing a signicant
correlation between supramodal responses and behavioral performance. The spatially-normalized results are projected onto single-subject hemisphere templates in Ta-
lairach space for the two experimental groups in a posterior view.
64 D. Bonino et al. / Neuropsychologia 68 (2015) 5970

Finally, to correlate supramodal brain responses with the be- 3. Results


havioral performances across sensory modalities, the neural re-
sponses to MCT conditions for both the tactile and auditory 3.1. Behavioral ndings
modalities of the two groups were considered in a single linear
trend analysis (run via 3dRegAna in AFNI) with the individual ac- Accuracy (percent mean 7 st. dev) for both groups during the
curacy for each experimental condition. Our volumes of interest MCT conditions were all signicantly above the chance level (50%;
were limited for each group to brain regions showing a within- po 0.001) sighted: auditory 82.3 7 6.9, tactile 78.5 75.4,
group stronger response to both tactile and auditory MCT as visual 90.5 77.8; Blind: auditory 72.3 7 10.9, tactile 81.2 79.4
compared to the control conditions (uncorrected voxel-wise (Fig. 1B). The repeated-measure, three-way ANOVA (age used as a
threshold of 0.05), to limit any possible non-independence error covariate) showed a signicant sensory modality  group interac-
(Kriegeskorte et al., 2009; Vul et al., 2009). Results have been tion (F(1,13) 10.5, p o0.006), but no signicant group (F(1,13) 0.2,
graphically reported in Fig. 3C at a voxel-wise threshold of 0.05. p4 0.6) or sensory modality (F(1,13) 3.5, p o0.08) effect. Post-hoc
comparisons showed a signicant within group effect in the au-
2.4.2.4. Differential brain response: between group comparisons. An ditory MCT, and revealed a signicant (p o0.04, Bonferroni cor-
across groups mixed-effect meta-analysis (equivalent to an un- rected) higher accuracy in sighted as compared to blind in-
paired T contrast) identied patterns of differential activation be- dividuals, while no group difference was found in the tactile MCT
tween sighted and congenitally blind groups for the tactile or the (Fig. 1B).
auditory MCT condition. In order to perform a SVC, we limited our The repeated-measure, two-way ANOVA in the sighted in-
dividuals revealed only a signicant modality effect (F(2,18) 10.35,
volume of interest to brain regions activated during both auditory
po 0.001), with a higher accuracy for the visual MCT as compared
and tactile MCT conditions (corrected po 0.05) across the sighted
to either the auditory (p o0.008, Bonferroni corrected) or tactile
and blind groups, with a voxel-wise threshold of 0.03 that resulted (p o0.001, Bonferroni corrected) MCT conditions; no differences in
in a minimum cluster volume 4 724 L, nearest-neighbor, for a accuracy were found between the auditory and tactile MCT con-
SVC corrected p value o 0.05 at cluster level. ditions (Fig. 1B).
Behavioral data for each of the control task conditions showed
2.4.2.5. Functional connectivity analysis. Each functional time-ser- an accuracy greater than 95%. Due to this performance at a ceiling
ies acquired during MCT execution was co-registered, temporally level, no differences across sensory modalities or groups were
aligned, spatially smoothed and normalized, as described above. found.
Then, data were resampled into 3 mm3 voxels, transformed into
Talairach space, and low-pass ltered (3dFourier) at 0.15 Hz to 3.2. Brain functional results
remove high frequency physiological artifacts including cardiac
and respiratory pulsatility (Birn et al., 2006). The six movement 3.2.1. Neural response to auditory, visual and tactile MCT and control
conditions
parameters estimated from the brain volume registration, and the
In brief, both congenitally blind and sighted volunteers showed
polynomial regressors that account for baseline shifts and linear/
a signicant (corrected p o0.05) recruitment of posterior parietal
quadratic/cubic drifts were mathematically removed from the
cortical areas-including the intraparietal, the superior and inferior
voxel timeseries (3dSynthesize) (Lund et al., 2006). To remove parietal cortex-across auditory, visual and tactile MCT, as com-
potential residual artifacts and reduce the probability of nding pared to a resting baseline (Fig. S1). Additionally, in sighted vo-
spurious functional correlations, white matter (WM) and cere- lunteers, auditory, tactile and visual MCT conditions activated a
brospinal uid (CSF) time-series were also regressed out (Ricciardi bilateral, though left prevalent, cortical pattern that included
et al., 2013). WM and CSF time courses were extracted from two dorsolateral and inferior frontal cortex, insula, ventral premotor,
ROIs (1 voxel radius) located in the corpus callosum and lateral and ventrotemporal regions. As expected, primary sensory cortical
ventricle, respectively, and identied on the common anatomical areas were enrolled according to the specic sensory modalities
template obtained by merging spatially normalized anatomical (see Supplementary materials, Fig. S1).
images of all subjects included in the analyses. For each subject, On the other hand, during the two control conditions, both
auditory and tactile tasks showed patterns of positive and negative
task-related scans obtained for tactile, auditory, and visual mod-
changes in brain activity as compared to the resting baseline si-
ality were concatenated separately. The seed ROIs were dened as
milar to those described for the respective MCT in both sighted
the overlapping clusters of response between sighted and blind and blind individuals.
group conjunction maps obtained as logical AND with the patterns
of activation within experimental condition, as detailed above. 3.2.2. Overlapping activations across experimental conditions
Whole brain functional connectivity was obtained by computing The voxel-by-voxel analysis to obtain a single subject con-
the Pearsons correlation coefcient between the mean BOLD junction map (Beauchamp et al., 2008) identied overlapping
time-course extracted from the seed ROI and the time-series of all clusters in bilateral posterior parietal and intraparietal regions in
other voxels of the brain. Fisher's Z transformation was used to both sighted and blind individuals (Table 2). Additionally, over-
convert correlation coefcients of each subject into Z scores. In lapping regions were found also in left middle frontal and pre-
order to determine signicant differences in functional con- motor areas in both groups, and in ventrotemporal, temporo-oc-
cipital and dorsal occipital regions in the blind group (Fig. 2A).
nectivity between congenitally blind and sighted individuals,
To determine the cortical regions that responded to all three
nonparametric MannWhitney tests, equivalent to unpaired t-
modalities, we also performed a conjunction analysis to create a
tests, were performed for each ROI and modality. As before, our
mixed-effects group map (Fig. 2B). The overlapping map showed
volume of interest limited to brain regions activated during both an active pattern of bilateral posterior parietal and intraparietal
auditory and tactile MCT conditions (corrected po 0.05) across the regions recruited across all the three sensory conditions by both
sighted and blind groups, with a SVC corrected p value o0.05 at sighted and congenitally blind individuals (Table 2). Additionally,
cluster level (voxelwise p o0.05, minimum volume of 1.053 L bilateral middle temporal, supplementary motor, bilateral middle
voxels). frontal and dorsal premotor areas were recruited in sighted
D. Bonino et al. / Neuropsychologia 68 (2015) 5970 65

Table 2 Table 2 (continued )


Cortical regions with signicant clusters of neural activity as identied by the
different contrasts. Brain areas Hem Sighted Blind
Coordinatesa Coordinates
Brain areas Hem Sighted Blind
Coordinatesa Coordinates x y z x y z

x y z x y z Middle frontal L  46 2 33

Overlapping activations across experimental conditions single subject


conjunction map Comparison between groups-MCT tactile modality
Posterior parietal/ L  37  44 39  32  41 44 Superior parietal/ R 26  54 42
intraparietal intraparietal
R 40  39 43 27  52 43 Middle occipital R 28  80 6
Middle frontal/ L  51 0 33
precentral
Overlapping activations across experimental conditions mixed-effect group
map
Posterior parietal/ L  33  51 45  21  55 46 Comparison between groups-MCT auditory modality
intraparietal Middle occipital L  17  84 15
R 34  44 46 25  57 42 R 31  78 4
Middle temporal L  47  48 7  35  64  13 Ventro-temporal L  32  63  11
R 50  50 5 34  55  19 R 32  56  13
Supplementary L 0 6 53 Middle frontal/ L  51 2 35
motor precentral
Middle frontal L  47 1 31
a
R 48 6 30 39 1 48 For each region, x, y, and z coordinates of the peak overlap from Talairach and
Dorsal premotor L  27  10 53 Tournoux atlas (Talairach & Tournoux, 1988) are provided. x distance in milli-
areas meters to the right ( ) or the left () side of the midline, ydistance anterior ( )
R 29 7 56 or posterior () to the anterior commissure z distance superior ( ) or inferior ()
Ventral and dorsal L  21  87 9 to a horizontal plane through the anterior and posterior commissures.
b
occipital This coordinate value in italic has been reported at a uncorrected po 0.05, as
R 5  93 2 described in Section 3.
R 29  80 6

Overlapping clusters in the conjunction analyses across experimental con-


individuals, while congenitally blind individuals showed addi-
ditions and between experimental groups
Posterior parietal/ L  27  57 45  27  57 45 tional bilateral ventral and dorsal occipital, middle temporal and
intraparietal right middle frontal clusters (Table 2).
R 30  53 44 30  53 44 Overlapping clusters in the conjunction analyses across ex-
perimental conditions and between experimental groups were
Comparison between experimental conditions: MCT4control tasks-auditor- found in bilateral posterior parietal and intraparietal regions
y tactile modalities (green clusters in Fig. 2B; Table 2).
Superior parietal/ L  22  71 46  25  49 40b
intraparietal
R 23  65 49 26  56 39 3.2.3. Comparison between experimental conditions: MCT vs. control
Middle frontal L  50 0 33 tasks
R 53 8 31 The within-group MCT vs. control comparisons identied brain
Precentral R 56  17 39 areas with a stronger response to both tactile and auditory MCT as
Supplementary R 3  20 68
motor
compared to the control conditions (Fig. 3A). Interestingly, even if
Anterior middle L  57  27 6 both groups relied on common superior parietal and intraparietal
temporal regions bilaterally, the within-group MCT vs. control condition
Fusiform and in- L  34  72  20  20  69  18 comparisons identied a distinct lateralization of the recruitment
ferior occipital
R 28  66  14
across this spatial processing network in the tactile and auditory
conditions.
In sighted individuals (Fig. 3A, left side and Table 2), bilateral
Comparison between experimental conditions: MCT4control tasks-auditory
modality superior parietal and intraparietal cortex, bilateral middle frontal
Superior parietal/ L  17  70 51 and right precentral clusters showed a signicantly stronger (SVC
intraparietal po 0.05) response to both auditory and tactile MCT as compared
R 26  55 39
to the control conditions. Vice versa, supplementary motor area
and paracentral cortex, and left anterior middle temporal, bilateral
Comparison between experimental conditions: MCT4control tasks-tactile fusiform and inferior occipital clusters showed a higher response
modality
to both auditory and tactile control conditions.
Superior parietal/ L  21  70 48
intraparietal In blind individuals (Fig. 3A, right side), brain areas with a
R 26 64 49 25  54 41 within-group signicantly stronger (SVC po0.05) response to both
auditory and tactile MCT as compared to the control conditions
Correlation between supramodal responses and behavioral performances were identied in the right superior parietal and intraparietal re-
Superior parietal/ L  14  71 51  31  44 34 gion and left middle occipital and lingual gyri. At an uncorrected
intraparietal threshold, a left superior parietal and intraparietal cluster also
L  37  43 35
showed a stronger response to MCT task as compared to the control
R 35  44 40 39  46 42
Inferior/middle L  49  60 6 conditions in blind individuals. A signicantly higher response in
temporal the right inferior/middle temporal cortex was found in the blind
R 55 58  13 group for the control conditions as compared to the MCT tasks.
66 D. Bonino et al. / Neuropsychologia 68 (2015) 5970

As an experimental group  condition interaction could not be analysis to determine patterns of differential activation between
directly assessed at a functional level due to the unbalanced sighted and congenitally blind groups for the tactile or the audi-
sample sizes, within-group MCT vs. control comparisons were also tory MCT condition (Fig. 4A). During the tactile MCT task, sig-
performed separately for the tactile and auditory modalities. In nicant (SVC cluster po 0.05; voxel-wise po 0.01) differences
particular, we characterized the extent of those parietal clusters were found between the two groups, with a greater activation in
with a stronger response to MCT as compared to the control task, the right superior parietal and intraparietal region and in right
as an indirect evaluation of the group-specic access to supra- middle-dorsal occipital clusters in blind individuals, while sighted
modal spatial processing regions for the two sensory modalities individuals showed a signicantly higher response in left middle
(Fig. 3B). frontal/precentral cortex. During the auditory MCT, a similar dif-
Sighted individuals showed a signicantly greater supramodal ferential pattern was found, but no differences in parietal regions
response in a left superior/intraparietal cluster for both tactile and were found. Blind individuals resulted in a signicantly higher
auditory conditions (Fig. 3B, Table 2). A right superior parietal activation of bilateral middle occipital and ventro-temporal cortex
cluster also showed a stronger response in sighted participants (Table 2), while sighted individuals relied more on the recruitment
during the tactile modality. of the left middle frontal/precentral cortex.
On the contrary, blind individuals showed signicantly greater For the functional connectivity comparison, the conjunction
intraparietal clusters located on the right hemisphere for both map (Fig. 2B) obtained by combining task-related group activation
tactile and auditory conditions (Fig. 3B, Table 2). maps for all the investigated sensory modalities revealed two
clusters located symmetrically in left and right superior parietal
3.2.4. Correlations between supramodal responses and behavioral cortex (Talairach x, y, and z coordinates:  24,  57, 45; 30,
performance  53, 44). These supramodal clusters were used as seed ROIs for
As described in the Methods, a linear trend analysis was per- whole brain functional connectivity computation for each group
formed to correlate the supramodal response specic to the MCTs and experimental condition. When using both the left and right
with the experimental behavioral outcomes. Specically, as com- parietal clusters as seed ROIs, blind individuals showed a sig-
pared to multisensory regions, a supramodal response should be nicantly higher connectivity strength from the parietal seeds to
expected to be higher across the MCTs as compared to the control left superior parietal/intraparietal regions and ventral and dorsal
conditions, and even to correlate with the behavioral performance occipital clusters, while sighted individuals to left middle frontal/
measures. The linear trend showed that bilateral, though prevalent precentral regions (Fig. 4B).
in the left hemisphere, superior parietal and intraparietal clusters
in both groups showed a neural response across the MCTs that
correlated to the individual accuracy levels (Fig. 3C and Table 2). In 4. Discussion
sighted individuals, also left inferior/middle temporal and middle
frontal clusters showed a signicant correlation between neural Individuals who lack vision since birth often show perceptual
responses and performance levels. and representational skills comparable to sighted individuals.
However, in tasks that involve complex spatial mental abilities,
3.2.5. Differential brain responses: between group comparisons of congenitally blind individuals may reveal an impaired spatial
functional activation and connectivity strength patterns analysis. In order to dissect the differential effects of the lack of
Brain responses during experimental tasks in the two groups visual experience on the behavioral and neural correlates of spatial
were compared by using an across groups mixed-effect meta- imagery sustained by distinct sensory modalities, in the present

Fig. 4. Between group comparisons of functional activation and connectivity strength patterns. Statistical maps showing signicantly different brain responses of functional
activation (A) and connectivity strength (B top: right parietal seed; bottom: left parietal seed) patterns between sighted and congenitally blind individuals for the two
sensory modalities. The spatially-normalized results are projected onto single-subject hemisphere templates in Talairach space for the two experimental groups. The ROI
spheres used as functional connectivity seeds are shown in light green. SP/IPS: superior parietal and intraparietal regions; MF/PM: middle frontal and premotor regions.
(For interpretation of the references to color in this gure legend, the reader is referred to the web version of this article.)
D. Bonino et al. / Neuropsychologia 68 (2015) 5970 67

study sighted and congenitally blind subjects were asked to per- space itself, and on the processing of sensorimotor information
form the same spatial angle discrimination task under distinct within specic frames of reference. Interestingly, our observation
sensory conditions, using visual, tactile and auditory stimuli, of a supramodal parietal role supports our perspective that, al-
respectively. though vision offers distinctive information for spatial processing,
Our ndings showed both common and differential behavioral individuals who are visually-deprived since birth show spatial
and functional responses between congenitally blind and sighted representation that are for the most part comparable to those in
subjects. Specically, from a behavioral point of view, we found sighted individuals, even for those cognitive domains that im-
that in the tactile based angle discrimination task, performance plicitly rely on mental spatial representations, such as number
did not differ between the two groups, while performance was processing or action planning (Cattaneo et al., 2010; Eger et al.,
signicantly impaired in the blind group when using the auditory 2003; Ricciardi et al., 2009, 2010; Zacks, 2008).
modality, in line with previous reports (Noordzij et al., 2007). In order to precisely dene the parietal areas involved in the
Then, we investigated the neural counterparts for these com- geometric in-plane representation tasks, different univariate
mon and distinct behavioral effects in spatial imagery across comparisons were conducted to isolate specic supramodal re-
sensory modalities and groups. sponses (Ricciardi et al., 2014a; Ricciardi and Pietrini, 2011). As the
First, we tested the hypothesis that the neural mechanisms that current experimental design does not allow to assess whether the
subserve angle spatial perception and imagery are supramodal in neural content of spatial information was truly shared across
nature. In addition, we predicted that these parietal cortical areas sensory modalities-for instance, as by performing a multivariate
would be recruited in the mental representation of spatial in- analysis (a depth discussion abouth this topic may be found in
formation acquired through non-visual sensory modalities both in Ricciardi and Pietrini, 2011; Ricciardi et al., 2014a, 2014b) , in the
sighted and in congenitally blind subjects, in a way related to their current protocol we expected that supramodal responses should
distinct performance levels. Consequently, differences in the pat- reasonably fulll the following three functional conditions.
terns of neural response in blind individuals between the tactile First, by denition, supramodal recruitment should be shared,
and auditory MCTs could be interpreted as functional correlates of that is, should overlap, across sensory modalities-visual, tactile
specic levels of performance, or mental strategies, when subjects and auditory-in both sighted and congenitally blind (auditory and
deal with the same spatial representation as conveyed through tactile modalities only) individuals. Indeed, the bilateral superior
different sensory modalities. parietal and intraparietal clusters reported here were commonly
recruited by both experimental groups.
4.1. Overlapping activations across sensory conditions and groups Second, supramodal clusters should show a content specic
reect supramodal responses in the parietal cortex response (i.e., signicantly higher responses during the MCTs as
compared to the control conditions) and also correlate with the
Superior parietal and intraparietal regions have been strongly behavioral performance levels across sensory modalities. This
involved in the perception, representation and processing of spa- second characteristic should differentiate supramodal from multi-
tially-coded information, independently from the sensory mod- sensory responses: indeed, neural responses in multisensory areas
ality through which this information is conveyed to the brain (e.g. equally overlap across modalities but in an independent way from
Bonino et al., 2008; Cattaneo et al., 2008; Ptito, 2005; Ricciardi the specic content of sensory information (Beauchamp et al.,
et al., 2006, 2007; Vanlierde et al., 2003; Weeks et al., 2000). Here, 2008; Ricciardi and Pietrini, 2011). In the present study, as com-
we expanded this scheme of a common and more abstract re- pared to control conditions, bilateral superior parietal and in-
presentation of spatial information to geometric in-plane re- traparietal clusters demonstrated signicantly higher responses
presentations. Specically, this experimental paradigm showed for angle representation across sensory modalities.
both that common clusters in superior parietal and intraparietal Finally, the linear trend analysis indicated that neural responses
cortex process perceptual features and sustain mental re- across the MCTs of bilateral superior parietal and intraparietal
presentation of spatial information as prompted by the three dif- clusters in both groups correlated to the individual accuracy le-
ferent sensory modalities (i.e., tactile, auditory and visual stimu- vels.. Therefore, superior parietal and intraparietal cortex t all the
lation) in sighted individuals, and that overlapping parietal re- three functional criteria required for a brain region to be dened as
sponses occur in individuals who lack sight since birth as well. supramodal.
These observations in both sighted and congenitally blind in- The supramodal parietal responses reported here closely
dividuals indicate that visual experience is not a necessary pre- overlap with the clusters of activation in precuneus, superior
requisite for the development of a functional neural architecture parietal and intraparietal cortex found during tactile (Bonino et al.,
within the parietal cortex, which indeed plays a more general role 2008) or auditory (Gougoux et al., 2009; Voss et al., 2008) pro-
in processing spatial information. In addition, these shared acti- cessing of spatial information, or spatial imagery (Vanlierde et al.,
vations in areas within the posterior parietal cortex provide sup- 2003) in congenitally/early blind individuals.
port to a common neural basis for the analysis of space in per- Our two groups also showed additional areas of shared brain
ception and imagery (Trojano et al., 2000). responses. Both the conjunction maps at individual and group
Overall, the superior parietal and intraparietal cortical areas levels showed in congenitally blind individuals an overlapping
appear to play a more general role in spatial representation. As a cross-modal recruitment in ventrotemporal, temporo-occipital and
matter of fact, the mental representation of several cognitive dorsal occipital regions across sensory modalities, as shown for a
functions, including the domains of number processing and wide gamut of non-visual perceptual and cognitive tasks (re-
mathematics, music, language, or learning, is spatial in format viewed, among others, in Cattaneo and Vecchi, 2011; Cattaneo
(Hubbard et al., 2005; Ricciardi et al., 2014b; Beecham et al., 2009). et al., 2008; Kupers et al., 2011b; Merabet and Pascual-Leone,
Moreover, spatial localization and representation are necessarily 2010; Noppeney, 2007; Pietrini et al., 2009; Ricciardi and Pietrini,
integrated in motion discrimination, motor planning and control, 2011; Collignon et al., 2011).
or action understanding (Grefkes and Fink, 2005; Johnson et al., In sighted individuals, a common response was also found in a
1996). Additionally, the ability to navigate in the surrounding middle frontal and precentral cluster, consistent with previous
space relates to individual spatial map processing (Cattaneo and fMRI studies using the MCT to examine visuospatial imagery
Vecchi, 2011; Ricciardi et al., 2010). Altogether, these spatial-re- (Formisano et al., 2002; Sack et al., 2002b; Trojano et al., 2000).
lated abilities critically rely on the mental representation of the This prefrontal area has been associated consistently with
68 D. Bonino et al. / Neuropsychologia 68 (2015) 5970

attentional and working memory processes with visual and non- participants, with the left hemisphere being mainly activated
visual stimuli in both sighted and blind individuals (Bonino et al., during the categorical encoding and the right in the coordinate
2008; Ricciardi et al., 2006). While blind individuals in our non- (metric) task (Baciu et al., 1999; Trojano et al., 2002). The func-
visual MCTs also recruited this cluster, in the sighted group the tional observations in sighted individuals on the lateralization of
midfrontal/precentral areas showed both a signicantly greater visuospatial representations suggest that blind individuals may
activation and a stronger connectivity with supramodal parietal employ compensatory cognitive mechanisms to overcome the
regions, maybe related to a more prominent role of these pre- limitations due to sight loss. In our protocol, a greater recruitment
frontal areas in the integration of sensory inputs coming from of right parietal regions occurred in blind individuals, in particular
different modalities. In turn, the absence of vision may determine when their performance was analogous to the sighted sample, i.e.,
a modication in the involvement of central functions and, more during the tactile-based spatial processing task. This additional
specically, of connections with parietal and intraparietal areas recruitment may be consistent with the hypothesis of a functional
(Leo et al., 2012). compensation of the right parietal cluster when the contribution
of the left parietal regions to spatial processing is insufcient, or
4.2. Access to supramodal spatial representation is modulated by (sensory) impaired (Sack et al., 2002b). In our case, the MCT es-
sensory experience and behavioral performance sentially involves a size comparison. Typically, during the auditory
task condition, most of the sighted participants would compare
During spatial perception and imagery, supramodal superior digital times by rst generating visual images of the two clocks
parietal and intraparietal regions were activated bilaterally. from the numerical/verbal cues, and then by mentally contrasting
Nonetheless, the within-group MCT vs. control task condition the angles formed by their hands. For blind individuals, though,
comparisons identied parietal clusters with a signicantly higher while the tactile condition of the mental clock task mainly requires
response to tactile and auditory MCT in the left hemisphere in a simpler perceptual comparison, the auditory mental clock task
sighted individuals, and in the right hemisphere in the con- condition relies on a more complex translation of the digital in-
genitally blind sample (Fig. 3A and B). Additionally, in a group formation into a symbolic representation of spatial differences. As
comparison, congenitally blind individuals showed a greater re- a matter of fact, the observed impaired behavioral performance in
sponse in the right superior parietal and intraparietal region the blinds during the auditory task is consistent with the fact that
during the tactile, but not during the auditory, MCT as compared to perceptual limitations related to the lack of visual inputs impair
sighted individuals. Finally, although spatial representation in behavioral performance when dealing with multiple spatial
congenitally blind individuals appeared to rely more on the right mental representations (Vecchi, 1998; Vecchi et al., 1995) and
parietal regions, supramodal parietal seeds resulted in a higher likely force blind individuals to rely, at a higher cognitive level, on
connectivity strength with left superior parietal/intraparietal re- partially different non-visual spatial processes (Noordzij et al.,
gions and occipito-temporo visual areas both during the tactile 2007; Vecchi, 1998), as we also conrmed at a functional level.
and auditory MCT tasks, as compared to sighted individuals. On the other hand, it cannot be excluded that this lateralization
Altogether, these results delineate a bilateral spatial re- may be more directly related to specic spatial representations in
presentation, which is left-dominant in sighted and right-domi- conditions of sensory-deprivation. Categorical-based, left-dominant
nant in congenitally blind individuals, respectively. In particular, spatial representation relies on a more global reconstruction of
both group activations and functional connectivity maps suggest mental images, which could be more typically related to vision. Co-
that blind individuals make a greater use of the right parietal ordinate evaluation is based on a metric spatially-organized assem-
regions when an effective spatial representation occurs, as mir- bling of multi-part mental images, is lateralized to the right parietal
rored by the behavioral differences between auditory and tactile cortex and could be more related to tactile (and maybe auditory)
MCTs. In fact, as blind individuals had an impaired performance processing in blind individuals (Kosslyn, 1994). Consistently with this
during the auditory, but not the tactile, spatial imagery task, the hypothesis, blind individuals have been recently shown to be speci-
right superior and intraparietal clusters showed signicantly cally impaired in the ability, that requires a metric representation of
higher responses in blind as compared to sighted individuals only auditory space, to judge the relative position of a sound source in a
during the tactile, but not the auditory, MCT condition. sequence of three spatially separated stimuli (Gori et al., 2014). The
Is this asymmetric response in parietal regions related to a specic impairment in a task requiring a well-calibrated auditory
distinct spatial mental representation (and strategy) in con- spatial representation (auditory space bisection) is consistent with
genitally blind individuals, or to an additional recruitment that the behavioral and functional observations of our protocol.
compensates for the lack of visual inputs?
Specic hemispheric differences in brain response during vi- 4.3. Limitations of the study
suospatial processes have been reported already in sighted in-
dividuals. Of interest, Sack et al. (2002a, 2002b) showed that, In the present experimental protocol, behavioral and functional
while a visual MCT activated bilaterally the superior parietal and data were acquired from relatively small samples of sighted and
intraparietal regions, only the subgroup of sighted individuals who congenitally blind subjects as compared to those frequently found
received repetitive transcranial magnetic stimulation (rTMS) to the nowadays in fMRI studies.
right parietal lobe resulted in an impaired visuospatial perfor- However, it should be kept in mind that individuals with con-
mance. No signicant differences were reported in the sham and genital blindness due to a peripheral cause represent an ex-
in the left hemisphere stimulation groups. This observation sug- ceptionally rare sample, and even more so when strict selection
gests an hemispheric asymmetry in the functional relevance of criteria from a medical (e.g., healthy, drug-free) and demographic
parietal regions in spatial performance with the right parietal (e.g., independent living conditions, socially integrated) perspec-
cluster being able to compensate for the suppression of the left tive are adopted. Moreover, all our congenitally blind volunteers
one, and showing a high lateralized cortical representation of had to be familiar with the use of traditional tactile Braille clocks.
some visuospatial functions (Sack et al., 2002b). Also, the different task conditions that comprised the experi-
Furthermore, additional pieces of evidence indicate that the mental paradigms were overall relatively demanding, and this
recruitment of parietal (and prefrontal) regions during spatial likely led to the loss of fMRI data from three-out of the original
processing of mental images show a pattern of relative later- group of nine-congenitally blind individuals due to excessive head
alization according to the specic cognitive computation used by movement during scanning.
D. Bonino et al. / Neuropsychologia 68 (2015) 5970 69

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