تصویرسازی فضایی متکی بر مستقل حسی، هر چند حساس، سازمان عملکردی حسی در درون قشر جداری: مطالعه FMRI تبعیض آمیز زاویه ای در افراد بینا و نابینای مادرزاد

Although vision offers distinctive information to space representation, individuals who lack vision since birth often show perceptual and representational skills comparable to those found in sighted individuals. However, congenitally blind individuals may result in impaired spatial analysis, when engaging in ‘visual’ spatial features (e.g., perspective or angle representation) or complex spatial mental abilities. In the present study, we measured behavioral and brain responses using functional magnetic resonance imaging in sighted and congenitally blind individuals during spatial imagery based on a modified version of the mental clock task (e.g., angle discrimination) and a simple recognition control condition, as conveyed across distinct sensory modalities: visual (sighted individuals only), tactile and auditory. Blind individuals were significantly less accurate during the auditory task, but comparable-to-sighted during the tactile task. As expected, both groups showed common neural activations in intraparietal and superior 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 connectivity patterns across experimental conditions demonstrated also a functional lateralization, in a way that correlated with the distinct behavioral performance in blind and sighted individuals. Specifically, 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 regions. In conclusions, intraparietal and superior parietal regions subserve supramodal spatial representations 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 performance and/or mental strategies adopted when they deal with the same spatial representation as conveyed through different sensory modalities.

Since the pivotal studies by Kosslyn in the seventies (e.g., Kosslyn, 1973), there is ample evidence that chronometric properties of mental images are shared with visual percepts. The role of vision in shaping and modulating these functions, as well as in influencing the development of the neural structures underlying these abilities, however, remains still to be fully defined. Although vision offers distinctive information for the representation 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 experience may have just limited effects on the perception and mental representation of space (Cattaneo et al., 2008 and Ricciardi et al., 2010). As a matter of fact, individuals who are visually-deprived since birth show similar levels of performance to sighted individuals in distinct spatial discrimination tasks, including navigation, number processing or action planning (Aleman et al., 2001, Cattaneo and Vecchi, 2011, Fleming et al., 2006, Ricciardi et al., 2010 and Vecchi, 1998). Neuropsychological, lesion and functional brain studies indicate that spatial perceptual abilities and spatial mental representations critically rely on posterior parietal regions (Ricciardi et al., 2010, Sack et al., 2002a, Sack et al., 2002b, Trojano et al., 2002 and Trojano et al., 2000). Interestingly, these cortical regions are activated during both perceptual and imagery tasks, regardless of the sensory modality through which such a spatial information has been acquired (Cattaneo et al., 2008, Ptito et al., 2011, Ricciardi et al., 2014a, Ricciardi et al., 2014b, Ricciardi et al., 2010 and Ricciardi and Pietrini, 2011). Furthermore, congenitally blind individuals recruit intraparietal and superior parietal regions during non-visual spatial processing and localization (Weeks et al., 2000), spatial imagery (Vanlierde et al., 2003), orientation discrimination (Ptito, 2005), spatial attention and memory (Bonino et al., 2008), and even numerical comparison (Szucs and Csepe, 2005) tasks. Altogether, these observations strongly suggest a more abstract, visual-independent sensory representation of spatial information in the human brain, that is, a supramodal functional organization. On the other hand, blind individuals do acquire a reduced amount of sensorial information, in terms of both classical ‘visual’ spatial features (e.g., perspective or angle representation) and their simultaneous and integrated perception, as compared to sighted ones (Cattaneo and Vecchi, 2008). At a behavioral level, these perceptual limitations result in impaired responses when individuals perform spatial imagery tasks that rely on visually-based representations, or that involve complex spatial mental abilities (Cattaneo et al., 2008, Gori et al., 2014 and Struiksma et al., 2009). For instance, performance differed between congenitally blind and sighted participants in a spatial-imagery task of angle discrimination, but not in a visually-based or auditory-based imagery tasks of object form (Noordzij et al., 2007). Similarly, dealing with multiple or three-dimensional spatial mental representations may be rather problematic for congenitally blind individuals (Vecchi, 1998 and Vecchi et al., 1995). Indeed, blind individuals develop their cognitive mechanisms through touch and hearing, which only allow for a sequential processing of information. This may force people who lack vision since birth to rely, at a higher cognitive level, on partially different non-visual spatial processes (Noordzij et al., 2007 and Vecchi, 1998). At a neural level, brain responses across distinct perceptual tasks in sighted and congenitally blind individuals show both similar patterns of activation within wide portions of association cortical areas (Ricciardi et al., 2014a) and a differential recruitment of primary visual cortical areas (Vanlierde et al., 2003), due to cross-modal plastic functional rearrangements in vision-related cortical areas (Kupers et al., 2011a and Ricciardi and Pietrini, 2011). Overall, these findings indicate that in the brain supramodal and 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 place despite the lack of visual input, whereas cross-modal plasticity is the functional rearrangement that occurs because of the lack of sight ( Ricciardi et al., 2014a and Ricciardi et al., 2014b). In the present study, we wished to examine to what extent (the lack of) visual experience and the specific features of the distinct sensory modalities may affect the brain functional architecture that sustains spatial imagery. Specifically, we measured brain responses in both sighted and congenitally blind individuals during an angle discrimination task in which stimuli were presented through the visual (sighted subjects only), tactile and auditory pathways. Previous studies showed that in sighted individuals angle size detection relies on a bilateral, though left-dominant, recruitment of posterior parietal regions (Formisano et al., 2002 and Trojano et al., 2000). Further, at a behavioral level, congenitally blind individuals showed significantly lower degrees of performance in a spatial-imagery task of angle discrimination as compared to sighted ones (Noordzij et al., 2007). Based on the observations discussed above, we predicted that spatial imagery would be associated with a shared supramodal functional response within the parietal cortical areas related to spatial perception, that is, this area would be recruited independently from visual experience and from the sensory channel used for angle spatial perception. At the same time, given the distinctive features of mental processing, as well as previous findings from distinct studies on spatial perception in sighted and congenitally blind individuals obtained in our own lab ( Bonino et al., 2008, Ricciardi et al., 2006 and Ricciardi et al., 2007), we also expected that within this common supramodal functional architecture, patterns of neural response would be shaped to some extent by visual experience and by the distinctive features of the specific sensory modality utilized to acquire spatial information.

Accuracy (percent mean±st. dev) for both groups during the MCT conditions were all significantly above the chance level (50%; p<0.001) – sighted: auditory=82.3±6.9, tactile=78.5±5.4, visual=90.5±7.8; Blind: auditory=72.3±10.9, tactile=81.2±9.4 ( Fig. 1B). The repeated-measure, three-way ANOVA (age used as a covariate) showed a significant sensory modality×group interaction (F(1,13)=10.5, p<0.006), but no significant group (F(1,13)=0.2, p>0.6) or sensory modality (F(1,13)=3.5, p<0.08) effect. Post-hoc comparisons showed a significant within group effect in the auditory MCT, and revealed a significant (p<0.04, Bonferroni corrected) higher accuracy in sighted as compared to blind individuals, while no group difference was found in the tactile MCT ( Fig. 1B). The repeated-measure, two-way ANOVA in the sighted individuals revealed only a significant modality effect (F(2,18)=10.35, p<0.001), with a higher accuracy for the visual MCT as compared to either the auditory (p<0.008, Bonferroni corrected) or tactile (p<0.001, Bonferroni corrected) MCT conditions; no differences in accuracy were found between the auditory and tactile MCT conditions ( Fig. 1B). Behavioral data for each of the control task conditions showed an accuracy greater than 95%. Due to this performance at a ceiling level, no differences across sensory modalities or groups were found.