Human Navigation Without and With Vision - the Role of Visual Experience and Visual Regions

Abstract

Human navigation relies on a wide range of visual retinotopic cortical regions yet the precise role that these regions play in navigation remains unclear. Are these regions mainly sensory input channels or also modality-independent spatial processing centers? Accordingly, will they be recruited for navigation also without vision, such as via audition? Will visual experience, or the lack thereof, affect this recruitment? Sighted, congenitally blind and sighted-blindfolded participants actively navigated virtual mazes during fMRI scanning before and after navigating them in the real world. Participants used the EyeCane visual-to-auditory navigation aid for non-visual navigation.We found that retinotopic regions, including both dorsal stream regions (e.g. V6) and primary regions (e.g. peripheral V1), were selectively recruited for non-visual navigation only after the participants mastered the EyeCane demonstrating rapid plasticity for non-visual navigation. The hippocampus, considered the navigation network’s core, displayed negative BOLD in all groups.Our results demonstrate the robustness of the retinotopic nodes modality-independent spatial role in non-visual human navigation to lifelong visual-deprivation, demonstrating that visual input during development is not required for their recruitment. Furthermore, our results with the blindfolded group demonstrate this recruitment’s robustness even to brief blindfolding, but only after brief training, demonstrating rapid task based plasticity. These results generalize the wider framework of task-selectivity rather than input-modality as a brain organization principle to dorsal-stream retinotopic areas and even for the first time to the primary visual cortex.HighlightsBoth visual and non-visual navigation recruit retinotopic regionsAfter training blindfolded subjects selectively recruit V1 & V6 for navigationThis holds also for participants with no visual experience (congenitally blind)The medial temporal lobe showed non-selective Negative BOLD in all groupsDeclaration of interestsAll authors declare that they have no conflicts of interests.

Are critical periods reversible in the adult brain? Insights on cortical specializations based on sensory deprivation studies

“…We also recently showed that V6, a classically known dorsal stream region, keeps responding to navigationrelated inputs in both congenitally blind and sighted blindfolded adults. Specifically, we showed that after short training with a minimalistic auditory SSD both groups of participants activated V6 during virtual maze auditory navigation (Maidenbaum et al, 2018) (Fig. 1).…”

“…This would predict for instance, the activation of foveally responsive regions for Braille reading or face processing (i.e., tasks requiring high-resolution shape analyses) in the deprived primary visual cortex (Amedi et al, 2017;Heimler and Amedi, 2020). Or the activation of peripherally responsive regions during navigation tasks (Maidenbaum et al, 2018), or during auditory localization tasks (i.e., tasks requiring low-resolution shape analyses) (Fig. 1).…”

Spatial Competence and Brain Plasticity in Congenital Blindness via Sensory Substitution Devices

“…In line with these results, CB participants, LB and blindfolded sighted controls learned to use an SSD to navigate in real-life size mazes. We observed that retinotopic regions, including both dorsal-stream regions (e.g., V6) and primary visual cortex regions (e.g., peripheral V1), were selectively recruited for non-visual navigation after the participants mastered the use of the SSD, demonstrating rapid plasticity for non-visual navigation (Maidenbaum et al, 2018). Moreover, the ability of participants to learn to use the SSD to detect and avoid obstacles was positively correlated with the volumes of a network commonly associated with navigation (Chebat et al, 2020; Figure 6D).…”

“…Thus, the resulting sensations are very different from vision in the sighted, and cannot genuinely replace a missing sense for all of its functions (Moraru and Boiangiu, 2016). This is also true for task specific sensory independent regions according to the task being completed (Kupers et al, 2010a;Matteau et al, 2010;Ptito et al, 2012;Striem-Amit et al, 2012a,b;Abboud et al, 2015;Maidenbaum et al, 2018). SSDs have not become widespread in their general use by the blind population (Loomis et al, 2010;Elli et al, 2014), for various practical reasons (Chebat et al, 2018a).…”

“…This process, known as amodality ( Heimler et al, 2015 ; Chebat et al, 2018b ) enables the recruitment of brain areas in a task specific, sensory independent fashion ( Cohen et al, 1997 ). The recruitment of task-specific brain nodes for shapes ( Ptito et al, 2012 ), motion ( Saenz et al, 2008 ; Ptito et al, 2009 ; Matteau et al, 2010 ; Striem-Amit et al, 2012b ), number-forms ( Abboud et al, 2015 ), body shapes ( Striem-Amit and Amedi, 2014 ), colors ( Steven et al, 2006 ), word shapes ( Striem-Amit et al, 2012a ), faces ( Likova et al, 2019 ), echolocation ( Norman and Thaler, 2019 ), and tactile navigation ( Kupers et al, 2010a ; Maidenbaum et al, 2018 ) is thought to represent mechanisms of brain plasticity ( Fine and Park, 2018 ; Singh et al, 2018 ) for specific amodal recruitment ( Ptito et al, 2008a ; Chebat et al, 2018b ; see Figure 2 ). The recruitment of the brain areas via SSDs not only shows that it is possible to supplement missing visual information, but that the brain treats the SSD information as if it were real vision, in the sense that it tries to extract the relevant sensory information for each specific task we are trying to accomplish (i.e., motion, colors, navigation, and other tasks illustrated in Figure 2 ).…”