Neural correlates of virtual route recognition in congenital blindness

Abstract

Despite the importance of vision for spatial navigation, blind subjects retain the ability to represent spatial information and to move independently in space to localize and reach targets. However, the neural correlates of navigation in subjects lacking vision remain elusive. We therefore used functional MRI (fMRI) to explore the cortical network underlying successful navigation in blind subjects. We first trained congenitally blind and blindfolded sighted control subjects to perform a virtual navigation task with the tongue display unit (TDU), a tactile-to-vision sensory substitution device that translates a visual image into electrotactile stimulation applied to the tongue. After training, participants repeated the navigation task during fMRI. Although both groups successfully learned to use the TDU in the virtual navigation task, the brain activation patterns showed substantial differences. Blind but not blindfolded sighted control subjects activated the parahippocampus and visual cortex during navigation, areas that are recruited during topographical learning and spatial representation in sighted subjects. When the navigation task was performed under full vision in a second group of sighted participants, the activation pattern strongly resembled the one obtained in the blind when using the TDU. This suggests that in the absence of vision, cross-modal plasticity permits the recruitment of the same cortical network used for spatial navigation tasks in sighted subjects.cross-modal plasticity | parahippocampus | sensory substitution | spatial navigation | visual cortex T he ability to navigate efficiently in large-scale environments was always a predicate for human survival, now applied to the particular challenges of living in a modern, urban society. Visual cues signaling the location of landmarks play a key role in facilitating the formation of spatial cognitive maps used for path finding in a visual setting (1, 2). Despite the importance of vision in spatial cognition, the abilities to recognize a traveled route and to represent spatial information are maintained in blind individuals (3-5), probably through tactile, auditory, and olfactory cues, as well as motion-related cues arising from the vestibular and proprioceptive systems.During successful navigation, spatial information needs to be encoded and retrieved. The role of the hippocampus for navigation in large-scale environments has been amply demonstrated in both animal (6-8) and human studies (9-11). Besides the hippocampus, several other areas in the posterior mesial lobe and posterior parietal, occipital, and infero-temporal cortices also play an important role in navigation (9,(12)(13)(14)(15)(16)(17).The neural correlates of navigation in congenital blindness remain elusive, in part owing to the difficulty in testing navigational skills of blind subjects within the setting of a functional brain imaging study. To circumvent this difficulty, we trained blind and sighted subjects in a spatial navigation task using the tongue display unit (TDU), a vis...

Neural Correlates of Human Echolocation of Path Direction During Walking

“…Importantly, in that study SPL was not only active during tactile route navigation but also when sighted control subjects executed the same task with full vision suggesting that parietal brain areas involved in navigation using vision can be recruited by other modalities in the blind. Our findings support and extend the results by Kupers et al (2010) showing that the SPL is also involved in spatial navigation based on echo sounds in blind and sighted people highlighting its function in multisensory spatial navigation.…”

“…Similar activations have been reported in a study where blind and blindfolded sighted subjects navigated a 2D virtual pathway using an electrotactile Tongue Display Unit suggesting that the SPL is part of a navigation and/or routerecognition network (Kupers et al, 2010). Importantly, in that study SPL was not only active during tactile route navigation but also when sighted control subjects executed the same task with full vision suggesting that parietal brain areas involved in navigation using vision can be recruited by other modalities in the blind.…”

“…In terms of brain activity, processing of tactile input, and in particular Braille reading, has also been linked to activity in striate and extra-striate visual areas (Büchel, 1998;Cohen et al, 1997;Sadato et al, 1996) . 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 9 With respect to navigation and/or spatial orientation specifically, it has been shown that blind people who have been trained to navigate in an environment using a sensory substitution device that transforms visual information into eletroctactile stimulation on the tongue perform superior to equally trained sighted blindfolded controls (Kupers et al, 2010). Furthermore, in the same study Kupers et al (2010) also showed that brain activation during route recognition in blind people coincided with locations of activations in sighted people performing the task based on visual information, and that the largest cluster of activation was in the PPC, in particular SPL, with other common activations in superior occipital cortex, cuneus and parahippocampus.…”

Tactile exploration of virtual objects for blind and sighted people: the role of beta 1 EEG band in sensory substitution and supramodal mental mapping

“…This is true when mapping spaces near and far from the body, for example, in manipulation and navigation, respectively. Both sighted and nonsighted people have shown such abilities using various sensory modalities (Kupers et al 2010;Seemungal et al 2007). It has been found that specific brain areas, including the hippocampus, posterior mesial lobe, and posterior parietal, occipital, and infero-temporal cortices, play an important role in spatial processing (Bird and Burgess 2008;Ekstrom et al 2003;Kravitz et al 2011;Latini-Corazzini et al 2010;Maguire et al 1998;Wascher et al 2009).…”

“…However, the mechanisms that could elicit a visuo-spatial representation from a tactile stimulation are necessarily complex, because discovering an object with touch implies the stimulation of several types of mechanoreceptors (Dahiya et al 2010), continuous motor programming and proprioception (Fiehler and Rösler 2010), and hypothesis generation and testing in the working memory (Kupers et al 2010). Classical visual neuroscience (Goodale et al 1991) hypothesizes that there are two distinct streams-one dorsal and one ventralfor cortical visual processing.…”