CHAPTER 27 - Blindness and Consciousness: New Light from the Dark

Current accounts of behavioral and neurocognitive correlates of plasticity in blindness are just beginning to incorporate the role of speech and verbal production. We assessed Vygotsky/Luria's speech mediation hypothesis, according to which speech activity can become a mediating tool for perception of complex stimuli, specifically, for encoding tactual/haptic spatial patterns which convey pictorial information (haptic pictures). We compared verbalization in congenitally totally blind (CTB) and age-matched sighted but visually impaired (VI) children during a haptic picture naming task which included two repeated, test-retest, identifications. The children were instructed to explore 10 haptic schematic pictures of objects (e.g., cup) and body parts (e.g., face) and provide (without experimenter's feedback) their typical name. Children's explorations and verbalizations were videorecorded and transcribed into audio segments. Using the Computerized Analysis of Language (CLAN) program, we extracted several measurements from the observed verbalizations, including number of utterances and words, utterance/word duration, and exploration time. Using the Word2Vec natural language processing technique we operationalized semantic content from the relative distances between the names provided. Furthermore, we conducted an observational content analysis in which three judges categorized verbalizations according to a rating scale assessing verbalization content. Results consistently indicated across all measures that the CTB children were faster and semantically more precise than their VI counterparts in the first identification test, however, the VI children reached the same level of precision and speed as the CTB children at retest. Overall, the task was harder for the VI group. Consistent with current neuroscience literature, the prominent role of speech in CTB and VI children's data suggests that an underlying cross-modal involvement of integrated brain networks, notably associated with Broca's network, likely also influenced by Braille, could play a key role in compensatory plasticity via the mediational mechanism postulated by Luria.

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.

For human and non-human primates, vision is one of the most privileged sensory channels used to interact with the environment. The importance of vision is strongly embedded in the organization of the primate brain as about one third of its cortical surface is involved in visual functions. It is therefore not surprising that the absence of vision from birth, or the loss of vision later in life, has huge consequences, both anatomically and functionally. Studies in animals and humans, conducted over the past few decades, have demonstrated that the absence of vision causes massive structural changes that take place not only in the visually deprived cortex but also in other brain areas. These studies have further shown that the visually deprived cortex becomes responsive to a wide variety of non-visual sensory inputs. Recent studies even showed a role of the visually deprived cortex in cognitive processes. At the behavioral level, increases in acuity for auditory and tactile processes have been reported. The study of the congenitally blind brain also offers a unique model to gain better insights into the functioning of the normal sighted brain and to understand to what extent visual experience is necessary for the brain to develop its functional architecture. Finally, the study of the blind brain allows us to investigate how consciousness develops in the absence of vision. How does the brain of someone who has never had any visual perception form an image of the external world? In this paper, we discuss recent findings from animal studies as well as from behavioural and functional brain imaging studies in sighted and blind individuals that address these questions.

While most of the research in blind individuals classically has focused on the compensatory plastic rearrangements that follow loss of sight, novel behavioral, anatomical and functional brain studies in individuals born deprived of sight represent a powerful tool to understand to what extent the brain functional architecture is programmed to develop independently from any visual experience. Here we review work from our lab and others, conducted in sighted and congenitally blind individuals, whose results indicate that vision is not a mandatory prerequisite for the brain cortical organization to develop and function. Similar cortical networks subtend visual and/or non-visual perception of form, space and movement, as well as action recognition, both in sighted and in congenitally blind individuals. These findings support the hypothesis of a modality independent, supramodal cortical organization. Visual experience, however, does play a role in shaping specific cortical sub-regions, as loss of sight is accompanied also by cross-modal plastic phenomena. Altogether, studying the blind brain is opening our eyes on how the brain develops and works.

High-resolution functional magnetic resonance imaging (fMRI) can be used to precisely identify blood oxygen level dependent (BOLD) activation of small structures within the brainstem not accessible with standard fMRI. A previous study identified a region within the pons exhibiting sustained neuromodulation due to electrical tongue stimulation, but was unable to precisely identify the neuronal structure involved. For this study, high-resolution images of neural activity induced by optic flow were acquired in nine healthy controls and nine individuals with balance dysfunction before and after information-free tongue stimulation. Subjects viewed optic flow videos to activate the structures of interest. Sub-millimeter in-plane voxels of structures within the posterior fossa were acquired using a restricted field of view. Whole-brain functional imaging verified that global activation patterns due to optic flow were consistent with previous studies. Optic flow activated the visual association cortices, the vestibular nuclei, and the superior colliculus, as well as multiple regions within the cerebellum. The anterior cingulate cortex showed decreased activity after stimulation, while a region within the pons had increased post-stimulation activity. These observations suggest the pontine region is the trigeminal nucleus and that tongue stimulation interfaces with the balance-processing network within the pons. This high-resolution imaging allows detection of activity within individual brainstem nuclei not possible using standard resolution imaging.

Adaptive neuroplastic changes have been well documented in congenitally blind individuals for the processing of tactile and auditory information. By contrast, very few studies have investigated olfactory processing in the absence of vision. There is ample evidence that the olfactory system is highly plastic and that blind individuals rely more on their sense of smell than the sighted do. The olfactory system in the blind is therefore likely to be susceptible to cross-modal changes similar to those observed for the tactile and auditory modalities. To test this hypothesis, we used functional magnetic resonance imaging to measure changes in the blood-oxygenation level-dependent signal in congenitally blind and blindfolded sighted control subjects during a simple odor detection task. We found several group differences in task-related activations. Compared to sighted controls, congenitally blind subjects more strongly activated primary (right amygdala) and secondary (right orbitofrontal cortex and bilateral hippocampus) olfactory areas. In addition, widespread task-related activations were found throughout the whole extent of the occipital cortex in blind but not in sighted participants. The stronger recruitment of the occipital cortex during odor detection demonstrates a preferential access of olfactory stimuli to this area when vision is lacking from birth. This finding expands current knowledge about the supramodal function of the visually deprived occipital cortex in congenital blindness, linking it also to olfactory processing in addition to tactile and auditory processing.