Abstract
This chapter reviews the most recent advances in sensory substitution and the neural correlates of navigation in congenital blindness . Studies have established the superior ability of congenitally blind (CB) participants with the aid of Sensory Substitution Devices (SSDs) to navigate new environments and detect the size and shape of obstacles in order to avoid them. These studies suggest that with training, CB can achieve a representation of space that is equivalent to that of the sighted. From a phenomenological point of view, sensation and perception provided by SSDs have been likened to real vision, but the question remains as to the subjective sensations (qualia) felt by users. We review recent theories on the phenomenological properties of sensory substitution and the recent literature on spatial abilities of participants using SSDs. From these different sources of research, we conclude that training-induced plastic changes enable task-specific brain activations. The recruitment of the primary visual cortex by nonvisual SSD stimulations and, the subsequent activations of associative visual cortices in the congenitally blind, suggest that the sensory information is treated in an amodal fashion; i.e.,: in terms of the task being performed rather than the sensory modality. These anatomical changes enable the embodiment of nonvisual information allowing SSD users to accomplish a multitude of “visual” tasks. We will emphasize here the abilities of CB individuals to navigate in real and virtual environments in spite of a large volumetric reduction in the posterior segment of the hippocampus , a key area involved in navigation . In addition, the superior behavioral performance of CB in a variety of sensory and cognitive tasks, combined with anatomical and functional MRI, underlines the susceptibility of the brain to training-induced plasticity.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 1.
The reader is referred to a film produced by Discovery channel on the various abilities developed by CB and LB participants using the TDU. « The Plastic Fantastic Brain » https://www.youtube.com/watch?v=IzmZArOryGk&t=5s.
- 2.
For more on this, please see the chapter, Harrar et al., The Multisensory Brain, Chap. 4 in this special edition).
References
Abboud S, Maidenbaum S, Dehaene S, Amedi A (2015). A number-form area in the blind. Nat Commun 6
Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6(6):823–829
Alary F, Goldstein R, Duquette M, Chapman CE, Voss P, Lepore F (2008) Tactile acuity in the blind: a psychophysical study using a two-dimensional angle discrimination task. Exp Brain Res 187(4):587–594
Amedi A, Chebat DR, Levy-Tzedek S, Buchs G, Maidenbaum S (2014) Returning sensory substitution to practical visual rehabilitation. Invest Ophthalmol Vis Sci 55(13):4146
Amedi A, Merabet LB, Camprodon J, Bermpohl F, Fox S, Ronen I, Kim DS, Pascual-Leone A (2008) Neural and behavioral correlates of drawing in an early blind painter: a case study. Brain Res 1242:252–262
Amedi A, Stern WM, Camprodon JA, Bermpohl F, Merabet L, Rotman S, Hermond C, Meijer P, Pascual-Leone A (2007) Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat Neurosci 10(6):687–689
Arnott SR, Thaler L, Milne JL, Kish D, Goodale MA (2013) Shape-specific activation of occipital cortex in an early blind echolocation expert. Neuropsychologia 51(5):938–949
Bach-y-Rita P, Collins CC, Saunders FA, White B, Scadden L (1969) Vision substitution by tactile image projection. Nature 221:963–964
Bach-y-Rita P (Ed.) (1972) Brain mechanisms in sensory substitution. Academic Press, New York
Bach-y-Rita P (1971) A tactile vision substitution system based on sensory plasticity. In: Visual prosthesis. Academic Press, New York
Baumann O, Mattingley JB (2013) Dissociable roles of the hippocampus and parietal cortex in processing of coordinate and categorical spatial information. Front Human Neurosci 8:73
Beaudry-Richard A, Harrar V, Auvray M, Spence C, Kupers R, Ptito M (2015) The multisensory substitution device: replacing vision with multisensory perception (poster). In: 16th Multisensory Research Forum (IMRF), Pisa, Italy, 13–16 June
Bhatlawande SS, Mukhopadhyay J, Mahadevappa M (2012) Ultrasonic spectacles and waist-belt for visually impaired and blind person. In: National conference on communications (NCC). IEEE, pp 1–4
Bird CM, Bisby JA, Burgess N (2012) The hippocampus and spatial constraints on mental imagery. Front Human Neurosci 6:142
Bohbot VD, Iaria G, Petrides M (2004) Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18(3):418
Borisoff JF, Elliott SL, Hocaloski S, Birch GE (2010) The development of a sensory substitution system for the sexual rehabilitation of men with chronic spinal cord injury. J Sex Med 7(11):3647–3658
Buchs G, Maidenbaum S, Amedi A (2014) Obstacle identification and avoidance using the ‘EyeCane’. EuroHaptics, LNCS 8619:13–18
Buchs G, Maidenbaum S, Amedi A, Levy-Tzedek S (2015) Virtually zooming-in with sensory substitution for blind users. In: International conference on Virtual rehabilitation proceedings (ICVR). IEEE, pp 133–134
Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641
Burgess N, Jackson A, Hartley T, O’keefe J (2000) Predictions derived from modelling the hippocampal role in navigation. Biol Cybern 83(3):301–312
Burton H, McLaren DG, Sinclair RJ (2006) Reading embossed capital letters: an fMRI study in blind and sighted individuals. Hum Brain Mapp 27(4):325–339
Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16(2):130–138
Byrne P, Becker S, Burgess N (2007) Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol Rev 114(2):340
Cappagli G, Gori M (2016) Auditory spatial localization: developmental delay in children with visual impairments. Res Dev Disabil 53:391–398
Cappagli G, Cocchi E, Gori M. (2015) Auditory and proprioceptive spatial impairments in blind children and adults. Develop Sci
Cattaneo Z, Vecchi T (2008) Supramodality effects in visual and haptic spatial processes. J Exp Psychol Learn Mem Cogn 34:631–642
Chan CC, Wong AW, Ting KH, Whitfield-Gabrieli S, He J, Lee T (2012) Cross auditory-spatial learning in early-blind individuals. Hum Brain Mapp 33(11):2714–2727
Chandler E, Worsfold J (2013) Understanding the requirements of geographical data for blind and partially sighted people to make journeys more independently. Appl Ergon 44(6):919–928
Chebat DR, Chen JK, Schneider F, Ptito A, Kupers R, Ptito M (2007) Alterations in right posterior hippocampus in early blind individuals. NeuroReport 18(4):329–333
Chebat DR, Maidenbaum S, Amedi A (2015) Navigation using sensory substitution in real and virtual mazes. PLoS ONE 10(6):e0126307
Chebat DR, Rainville C, Kupers R, Ptito M (2007) Tactile—‘visual’ acuity of the tongue in early blind individuals. NeuroReport 18(18):1901–1904
Chebat DR, Schneider FC, Kupers R, Ptito M (2011) Navigation with a sensory substitution device in congenitally blind individuals. NeuroReport 22(7):342–347
Chiou R, Stelter M, Rich AN (2013) Beyond colour perception: auditory–visual synaesthesia induces experiences of geometric objects in specific locations. Cortex 49(6):1750–1763
Cohen L, Dehaene S, Naccache L, Lehéricy S, Dehaene-Lambertz G, Hénaff MA, Michel F (2000) The visual word form area. Brain 123(2):291–307
Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Faiz L, Dambrosia J, Hallett M (1997) Functional relevance of cross-modal plasticity in blind humans. Nature 389(6647), 180–183
Collignon O, Lassonde M, Lepore F, Bastien D, Veraart C (2007) Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects. Cereb Cortex 17(2):457–465
Collignon O, Renier L, Bruyer R, Tranduy D, Veraart C (2006) Improved selective and divided spatial attention in early blind subjects. Brain Res 1075(1):175–182
Committeri G, Galati G, Paradis AL, Pizzamiglio L, Berthoz A, LeBihan D (2004) Reference frames for spatial cognition: different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. J Cogn Neurosci 16(9):1517–1535
Compton DM, Griffith HR, McDaniel WF, Foster RA, Davis BK (1997) The flexible use of multiple cue relationships in spatial navigation: a comparison of water maze performance following hippocampal, medial septal, prefrontal cortex, or posterior parietal cortex lesions. Neurobiol Learn Mem 68(2):117–132
Deroy O, Auvray M (2014) A crossmodal perspective on sensory substitution. Percep Modalities 327–349
Desimone R (1991) Face-selective cells in the temporal cortex of monkeys. J Cogn Neurosci 3(1):1–8
Deutschländer A, Stephan T, Hüfner K, Wagner J, Wiesmann M, Strupp M, Brandt T, Jahn K (2009) Imagined locomotion in the blind: an fMRI study. Neuroimage 45(1):122–128
Deutschländer A, Stephan T, Hüfner K, Wagner J, Wiesmann M, Strupp M, Brandt T, Jahn K (2009) Vestibular cortex activation during locomotor imagery in the blind. Ann NY Acad Sci 1164(1):350–352
Dietrich S, Hertrich I, Ackermann H (2013) Training of ultra-fast speech comprehension induces functional reorganization of the central-visual system in late-blind humans. Front Hum Neurosci 7(701):10–3389
Dilks DD, Julian JB, Paunov AM, Kanwisher N (2013) The occipital place area is causally and selectively involved in scene perception. J Neurosci 33(4):1331–1336
Doeller CF, Barry C, Burgess N (2010) Evidence for grid cells in a human memory network. Nature 463(7281):657–661
Doeller CF, King JA, Burgess N (2008) Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc Natl Acad Sci 105(15):5915–5920
Doucet ME, Guillemot JP, Lassonde M, Gagné JP, Leclerc C, Lepore F (2005) Blind subjects process auditory spectral cues more efficiently than sighted individuals. Exp Brain Res 160(2):194–202
Downing PE, Jiang Y, Shuman M, Kanwisher N (2001) A cortical area selective for visual processing of the human body. Science 293(5539):2470–2473
Duarte IC, Ferreira C, Marques J, Castelo-Branco M (2014) Anterior/posterior competitive deactivation/activation dichotomy in the human hippocampus as revealed by a 3D navigation task. PLoS ONE 9(1):e86213
Dunai L, Peris-Fajarnés G, Lluna E, Defez B (2013) Sensory navigation device for blind people. J Navig 66(03):349–362
D’Angiulli AMEDEO, Waraich P (2002) Enhanced tactile encoding and memory recognition in congenital blindness. Int J Rehabil Res 25(2):143–145
Ekstrom AD (2015) Why vision is important to how we navigate. Hippocampus 25(6):731–735
Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425(6954):184–188
Elli GV, Benetti S, Collignon O (2014) Is there a future for sensory substitution outside academic laboratories? Multisensory Res 27(5–6):271–291
Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12(10):388–396
Epstein R, Harris A, Stanley D, Kanwisher N (1999) The parahippocampal place area: recognition, navigation, or encoding? Neuron 23(1):115–125
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601
Epstein RA, Parker WE, Feiler AM (2007) Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27(23):6141–6149
Epstein RA, Vass LK (2014) Neural systems for landmark-based wayfinding in humans. Philos Trans R Soc Lond B Biol Sci 369(1635):20120533
Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N (2015) Three-dimensional head-direction coding in the bat brain. Nature 517(7533):159–164
Finocchietti S, Cappagli G, Gori M (2015) Encoding audio motion: spatial impairment in early blind individuals. Front Psychol 6
Fornazzari L, Fischer CE, Ringer L, Schweizer TA (2012) “Blue is music to my ears”: multimodal synesthesias after a thalamic stroke. Neurocase 18(4):318–322
Fortin M, Voss P, Lord C, Lassonde M, Pruessner J, Saint-Amour D, Rainville C, Lepore F (2008) Wayfinding in the blind: larger hippocampal volume and supranormal spatial navigation. Brain 131(11):2995–3005
Foster DJ, Knierim JJ (2012) Sequence learning and the role of the hippocampus in rodent navigation. Curr Opin Neurobiol 22(2):294–300
Gagnon L, Schneider FC, Siebner HR, Paulson OB, Kupers R, Ptito M (2012) Activation of the hippocampal complex during tactile maze solving in congenitally blind subjects. Neuropsychologia 50(7):1663–1671
Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N (2015) Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat Rev Neurosci 16(2):94–108
Giudice NA, Betty MR, Loomis JM (2011) Functional equivalence of spatial images from touch and vision: Evidence from spatial updating in blind and sighted individuals. J Exp Psychol Learn Mem Cogn 37(3):621
Giudice NA, Klatzky RL, Bennett CR, Loomis JM (2013) Perception of 3-D location based on vision, touch, and extended touch. Exp Brain Res 224(1):141–153
Giudice NA, Tietz JD (2008) Learning with virtual verbal displays: effects of interface fidelity on cognitive map development. In: International conference on spatial cognition. Springer, Berlin, pp 121–137
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25
Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP (2005) Effects of hippocampus sub-regional lesions for metric and topological spatial information processing. Soc Neurosci, Abstr
Gori M, Sandini G, Martinoli C, Burr DC (2014) Impairment of auditory spatial localization in congenitally blind human subjects. Brain 137(1):288–293
Gougoux F, Lepore F, Lassonde M, Voss P, Zatorre RJ, Belin P (2004) Neuropsychology: pitch discrimination in the early blind. Nature 430(6997):309
Greicius MD, Krasnow B, Boyett-Anderson JM, Eliez S, Schatzberg AF, Reiss AL, Menon V (2003) Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study. Hippocampus 13(1):164–174
Guderian S, Dzieciol AM, Gadian DG, Jentschke S, Doeller CF, Burgess N, Mishkin M, Vargha-Khadem F (2015) Hippocampal volume reduction in humans predicts impaired allocentric spatial memory in virtual-reality navigation. J Neurosci 35(42):14123–14131
Hackert VH, den Heijer T, Oudkerk M, Koudstaal PJ, Hofman A, Breteler MMB (2002) Hippocampal head size associated with verbal memory performance in nondemented elderly. Neuroimage 17(3):1365–1372
Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801–806
Hamid SN, Stankiewicz B, Hayhoe M (2010) Gaze patterns in navigation: encoding information in large-scale environments. J Vision 10(12):28
Hamilton RH, Pascual-Leone A, Schlaug G (2004) Absolute pitch in blind musicians. NeuroReport 15(5):803–806
Hamilton-Fletcher G, Obrist M, Watten P, Mengucci M, Ward J (2016) I always wanted to see the night sky: blind user preferences for Sensory Substitution Devices
Hartcher-O’Brien J, Auvray M (2014) The process of distal attribution illuminated through studies of sensory substitution. Multisensory Res 27(5–6):421–441
Hartcher-O’Brien J, Auvray M, Hayward V (2015) Perception of distance-to-obstacle through time-delayed tactile feedback. In World Haptics Conference (WHC), 2015 IEEE (pp 7–12). IEEE
Hassabis D, Chu C, Rees G, Weiskopf N, Molyneux PD, Maguire EA (2009) Decoding neuronal ensembles in the human hippocampus. Curr Biol 19(7):546–554
Haxby JV, Grady CL, Horwitz B, Ungerleider LG, Mishkin M, Carson RE, Herscovitch P, Schapiro MB, Rapoport SI (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Nat Acad Sci 88(5):1621–1625
He C, Peelen MV, Han Z, Lin N, Caramazza A, Bi Y (2013) Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience. Neuroimage 79:1–9
Heimler B, Striem-Amit E, Amedi A (2015) Origins of task-specific sensory-independent organization in the visual and auditory brain: neuroscience evidence, open questions and clinical implications. Curr Opin Neurobiol 35:169–177
Herman JF, Herman TG, Chatman SP (1983) Constructing cognitive maps from partial information: a demonstration study with congenitally blind subjects. J Vis Impair Blindness
Hersh MA, Johnson MA (2010) A robotic guide for blind people. Part 1. A multi-national survey of the attitudes, requirements and preferences of potential end-users. Appl Bion Biomech 7(4):277–288
Hill J, Black J (2003) The miniguide: a new electronic travel device. J Vis Impair Blindness 97(10):1–6
Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425(6960):828–832
Iachini T, Ruggiero G (2010) The role of visual experience in mental scanning of actual pathways: evidence from blind and sighted people. Perception 39(7):953–969
Iachini T, Ruggiero G, Ruotolo F (2014) Does blindness affect egocentric and allocentric frames of reference in small and large scale spaces? Behav Brain Res 273:73–81
Iaria G, Chen JK, Guariglia C, Ptito A, Petrides M (2007) Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 25(3):890–899
Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J Neurosci 23(13):5945–5952
Ione A, Tyler C (2004) Neuroscience, history and the arts synesthesia: is F-sharp colored violet? J Hist Neurosci 13(1):58–65
Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei X, Kahana MJ (2013) Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci 16(9):1188–1190
Jahn K, Wagner J, Deutschländer A, Kalla R, Hüfner K, Stephan T, Brandt T (2009) Human hippocampal activation during stance and locomotion. Ann NY Acad Sci 1164(1):229–235
Julian JB, Ryan J, Hamilton RH, Epstein RA (2016) The occipital place area is causally involved in representing environmental boundaries during navigation. Curr Biol 26(8):1104–1109
Kamps FS, Julian JB, Kubilius J, Kanwisher N, Dilks DD (2016) The occipital place area represents the local elements of scenes. NeuroImage 132:417–424
Karcher S, Fenzlaff S, Hartmann D, Nagel S, Konig P (2012) Sensory augmentation for the blind. Front Hum Neurosci 1(6):37. doi:10.3389/fnhum.2012.00037
Kaspar K, König S, Schwandt J, König P (2014) The experience of new sensorimotor contingencies by sensory augmentation. Conscious Cogn 28:47–63
Kay L (1974) A sonar aid to enhance spatial perception of the blind: engineering design and evaluation. Radio Electron Eng 44(11):605–627
King AJ (2014) What happens to your hearing if you are born blind? Brain 137(1):6–8
King AJ (2009) Visual influences on auditory spatial learning. Philos Trans R Soc London B Biol Sci 364(1515):331–339
Kober SE, Wood G, Kampl C, Neuper C, Ischebeck A (2014) Electrophysiological correlates of mental navigation in blind and sighted people. Behav Brain Res 273:106–115
Kosslyn SM, Chabris CF, Marsolek CJ, Koenig O (1992) Categorical versus coordinate spatial relations: computational analyses and computer simulations. J Exp Psychol Hum Percept Perform 18(2):562
Kosslyn SM, Koenig O, Barrett A, Cave CB, Tang J, Gabrieli JD (1989) Evidence for two types of spatial representations: hemispheric specialization for categorical and coordinate relations. J Exp Psychol Hum Percept Perform 15(4):723
Krishna S, Bala S, McDaniel T, McGuire S, Panchanathan S (2010) VibroGlove: an assistive technology aid for conveying facial expressions. In: Proceedings of the 28th of the international conference extended abstracts on human factors in computing systems. ACM, Atlanta, Georgia, USA, pp 3637–3642. doi:10.1145/1753846.1754031
Kupers R, Chebat DR, Madsen KH, Paulson OB, Ptito M (2010) Neural correlates of virtual route recognition in congenital blindness. Proc Natl Acad Sci 107(28):12716–12721
Kupers R, Ptito M (2014) Compensatory plasticity and cross-modal reorganization following early visual deprivation. Neurosci Biobehav Rev 41:36–52
Kupers R, Pietrini P, Ricciardi E, Ptito M (2011) The nature of consciousness in the visually deprived brain. Front Psychol 2(4)
Lacey S, Sathian K (2014) Visuo-haptic multisensory object recognition, categorization, and representation. Front Psychol 5:730
Lacey S, Stilla R, Sreenivasan K, Deshpande G, Sathian K (2014) Spatial imagery in haptic shape perception. Neuropsychologia 60:144–158
Lahav O (2006) Using virtual environment to improve spatial perception by people who are blind. Cyberpsychology Behav 9(2):174–177
Law CT, Gold JI (2008) Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area. Nat Neurosci 11(4):505–513
Leporé N, Shi Y, Lepore F, Fortin M, Voss P, Chou YY, Lord C, Lassonde M, Dinov ID, Toga AW, Thompson PM (2009) Pattern of hippocampal shape and volume differences in blind subjects. Neuroimage 46(4):949–957
Lessard N, Pare M, Lepore F, Lassonde M (1998) Early-blind human subjects localize sound sources better than sighted subjects. Nature 395(6699):278–280
Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29(31):9771–9777
Levy-Tzedek S, Hanassy S, Abboud S, Maidenbaum S, Amedi A (2012) Fast, accurate reaching movements with a visual-to-auditory sensory substitution device. Restorative Neurol Neurosci 30(4):313–323
Lewald J (2013) Exceptional ability of blind humans to hear sound motion: implications for the emergence of auditory space. Neuropsychologia 51(1):181–186
Loomis JM, Klatzky RL, Giudice NA (2012) Sensory substitution of vision: importance of perceptual and cognitive processing. CRC Press, Boca Raton, pp 162–191
Loomis JM, Klatzky RL, Golledge RG, Cicinelli JG, Pellegrino JW, Fry PA (1993) Nonvisual navigation by blind and sighted: assessment of path integration ability. J Exp Psychol Gen 122(1):73
Loomis JM, Wiener WR, Welsh RL, Blasch BB (2010) Sensory substitution for orientation and mobility: what progress are we making? In: Guth DA, Rieser JJ, Ashmead DH (eds) Perceiving to move and moving to perceive: control of locomotion by students with vision loss. Foundations of Orientation and Mobility (History and Theory), pp 7–10
Lynch K (1960) The image of the city, vol 11. MIT Press, Cambridge
Maguire EA, Frackowiak RSJ, Frith CD (1996) Learning to find your way: a role for the human hippocampal formation. Proc R Soc Lond B Biol Sci 263(1377):1745–1750
Maguire EA, Frackowiak RS, Frith CD (1997) Recalling routes around London: activation of the right hippocampus in taxi drivers. J Neurosci 17(18):7103–7110
Maguire EA, Frith CD, Burgess N, Donnett JG, O’Keefe J (1998) Knowing where things are: parahippocampal involvement in encoding object locations in virtual large-scale space. Cogn Neurosci J 10(1):61–76
Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD (2000) Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci 97(8):4398–4403
Maguire EA, Woollett K, Spiers HJ (2006) London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16(12):1091–1101
Maidenbaum S, Abboud S, Amedi A (2014) Sensory substitution: closing the gap between basic research and widespread practical visual rehabilitation. Neurosci Biobehav Rev 41:3–15
Maidenbaum S, Abboud S, Buchs G, Amedi A (2015) Blind in a virtual world: using sensory substitution for generically increasing the accessibility of graphical virtual environments. In Virtual Reality (VR), 2015 IEEE (pp 233–234). IEEE
Maidenbaum S, Arbel R, Abboud S, Chebat D, Levy-Tzedek S, Amedi A (2012) Virtual 3D shape and orientation discrimination using point distance information. In Proceedings of the 9th international conference disability, virtual reality & associated technologies, pp 471–474
Maidenbaum S, Buchs G, Abboud S, Lavi-Rotbain O, Amedi A (2016) Perception of graphical virtual environments by blind users via sensory substitution. PLoS ONE 11(2):e0147501
Maidenbaum S, Hanassy S, Abboud S, Buchs G, Chebat DR, Levy-Tzedek S, Amedi A (2014) The “EyeCane”, a new electronic travel aid for the blind: Technology, behavior & swift learning. Restorative Neurol Neurosci 32(6):813–824
Maidenbaum S, Levy-Tzedek S, Chebat DR, Amedi A (2013) Increasing accessibility to the blind of virtual environments, using a virtual mobility aid based on the “EyeCane”: feasibility study. PLoS ONE 8(8):e72555
Maidenbaum S, Levy-Tzedek S, Chebat DR, Namer-Furstenberg R, Amedi A (2014) The effect of extended sensory range via the EyeCane sensory substitution device on the characteristics of visionless virtual navigation. Multisensory Res 27(5–6):379–397
Maller JJ, Thomson RH, Ng A, Mann C, Eager M, Ackland H, Fitzgerald PB, Egan G, Rosenfeld JV (2016) Brain morphometry in blind and sighted subjects. J Clin Neurosci
Mann S, Huang J, Janzen R, Raymond L, Rampersad V, Chen A, Doha T (2011) Blind navigation with a wearable range camera and vibrotactile helmet. In: Proceedings of the 19th ACM international conference on multimedia, pp 1325–1328
Marks LE (1975) On colored-hearing synesthesia: cross-modal translations of sensory dimensions. Psychol Bull 82(3):303
Marston JR, Church RL (2005) A relative access measure to identify barriers to efficient transit use by persons with visual impairments. Disabil Rehabil 27(13):769–779
Matteau I, Kupers R, Ricciardi E, Pietrini P, Ptito M (2010) Beyond visual, aural and haptic movement perception: hMT+ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals. Brain Res Bull 82(5):264–270
Matteau I, Kupers R, Ptito M (2008) Tactile shape recognition through the tongue in the congenitally blind. In: FENS. Abstracts, vol 4, pp 153–158
McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102(3):419
Meijer PB (1992) An experimental system for auditory image representations. IEEE Trans Biomed Eng 39:112–121
Merabet LB, Connors EC, Halko MA, Sánchez J (2012) Teaching the blind to find their way by playing video games. PLoS ONE 7(9):e44958
Merabet LB, Sánchez J (2016) Development of an audio-haptic virtual interface for navigation of large-scale environments for people who are blind. In: International conference on universal access in human-computer interaction. Springer International Publishing, Berlin, pp 595–606
Millar S (1988) Models of sensory deprivation: the nature/nurture dichotomy and spatial representation in the blind. Int J Behav Dev 11(1):69–87
Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46(3):774–785
Montello DR, Sas C (2006) Human factors of wayfinding in navigation
Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Neuroscience 31(1):69
Muessig L, Hauser J, Wills TJ, Cacucci F (2016) Place cell networks in pre-weanling rats show associative memory properties from the onset of exploratory behavior. Cereb Cortex 174
Murphy MC, Fisher C, Kim SG, Schuman JS, Nau AC, Chan KC (2014) Top down influence on the visual cortex of the blind during auditory sensory substitution. In: Proceedings of International Society for Magnetic Resonance in Medicine, vol 22, p 579
Nau AC, Pintar C, Fisher C, Jeong JH, Jeong K (2014) A standardized obstacle course for assessment of visual function in ultra low vision and artificial vision. J Visualized Exp (JoVE) 84:e51205–e51205
Nitz DA (2006) Tracking route progression in the posterior parietal cortex. Neuron 49(5):747–756
Nitz D (2009) Parietal cortex, navigation, and the construction of arbitrary reference frames for spatial information. Neurobiol Learn Mem 91(2):179–185
Noppeney U (2007) The effects of visual deprivation on functional and structural organization of the human brain. Neurosci Biobehav Rev 31(8):1169–1180
Noë A (2010) Vision without representation. In: Perception, action, and consciousness: sensorimotor dynamics and two visual systems, pp 245–256
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map, vol 3. Clarendon Press, Oxford, pp 483–484
O’Regan JK, Noë A (2001) A sensorimotor account of vision and visual consciousness. Behav Brain Sci 24(05):939–973
Passini R, Proulx G, Rainville C (1990) The spatio-cognitive abilities of the visually impaired population. Environ Behav 22(1):91–118
Patla AE, Prentice SD, Gobbi LT (1996) Visual control of obstacle avoidance during locomotion: strategies in young children, young and older adults. Adv Psychol 114:257–277
Patla AE, Vickers JN (1997) Where and when do we look as we approach and step over an obstacle in the travel path? NeuroReport 8(17):3661–3665
Phillips B, Zhao H (1993) Predictors of assistive technology abandonment. Assistive Technol 5(1):36–45
Pietrini P, Ptito M, Kupers R (2009) Blindness and consciousness: new light from the dark. In: The neurology of consciousness: Cognitive neuroscience and neuropathology, pp 360–374
Pissaloux E, Velazquez R, Hersh M, Uzan G (2016) Towards a cognitive model of human mobility: an investigation of tactile perception for use in mobility devices. J Navig 1–17
Poirier C, Collignon O, DeVolder AG, Renier L, Vanlierde A, Tranduy D, Scheiber C (2005) Specific activation of the V5 brain area by auditory motion processing: an fMRI study. Cogn Brain Res 25(3):650–658
Proulx MJ (2010) Synthetic synaesthesia and sensory substitution. Conscious Cogn 19(1):501–503
Proulx MJ, Pasqualotto A, Taya S (2012) The role of visual experience for spatial numerical associations. Seeing Perceiving 25:222-222
Ptito M, Matteau I, Gjedde A, Kupers R (2009) Recruitment of the middle temporal area by tactile motion in congenital blindness. NeuroReport 20(6):543–547
Ptito M, Moesgaard SM, Gjedde A, Kupers R (2005) Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. Brain 128(3):606–614
Ptito M, Schneider FC, Paulson OB, Kupers R (2008) Alterations of the visual pathways in congenital blindness. Exp Brain Res 187(1):41–49
Ptito M, Matteau I, Zhi Wang A, Paulson OB, Siebner HR, Kupers R (2012) Crossmodal recruitment of the ventral visual stream in congenital blindness. Neural Plast
Rao AS, Gubbi J, Palaniswami M, Wong E (2016, May). A vision-based system to detect potholes and uneven surfaces for assisting blind people. In 2016 IEEE International Conference on Communications (ICC)(pp 1–6). IEEE
Reich L, Szwed M, Cohen L, Amedi A (2011) A ventral visual stream reading center independent of visual experience. Curr Biol 21(5):363–368
Reich L, Maidenbaum S, Amedi A (2012) The brain as a flexible task machine: implications for visual rehabilitation using noninvasive vs. invasive approaches. Curr Opin Neurol 25(1):86–95
Reynolds Z, Glenney B (2009) Interactive training for sensory substitution devices. In: Proceedings of AP-CAP, pp 131–134
Roder B, Teder-SaÈlejaÈrvi W, Sterr A, RoÈsler F, Hillyard SA, Neville HJ (1999) Improved auditory spatial tuning in blind humans. Nature 400(6740):162–166
Rolls ET, O’Mara SM (1995) View-responsive neurons in the primate hippocampal complex. Hippocampus 5(5):409–424
Sadato N, Pascual-Leone A, Grafman J, Deiber MP, Ibanez V, Hallett M (1998) Neural networks for Braille reading by the blind. Brain 121(7):1213–1229
Sadeghi SG, Minor LB, Cullen KE (2012) Neural correlates of sensory substitution in vestibular pathways following complete vestibular loss. J Neurosci 32(42):14685–14695
Saenz M, Lewis LB, Huth AG, Fine I, Koch C (2008) Visual motion area MT+/V5 responds to auditory motion in human sight-recovery subjects. J Neurosci 28(20):5141–5148
Sathian K, Zangaladze A (2002) Feeling with the mind’s eye: contribution of visual cortex to tactile perception. Behav Brain Res 135(1):127–132
Sathian K, Lacey S (2008) Visual cortical involvement during tactile perception in blind and sighted individuals. Blindness and brain plasticity in navigation and object perception. Erlbaum, Mahwah, pp 113–125
Schinazi VR, Epstein RA (2010) Neural correlates of real-world route learning. Neuroimage 53(2):725–735
Schinazi VR, Thrash T, Chebat DR (2016) Spatial navigation by congenitally blind individuals. Wiley Interdisc Rev Cogn Sci 7(1):37–58
Segond H, Weiss D, Sampaio E (2005) Human spatial navigation via a visuo-tactile sensory substitution system. Perception 34(10):1231–1249
Shimony JS, Burton H, Epstein AA, McLaren DG, Sun SW, Snyder AZ (2006) Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb Cortex 16(11):1653–1661
Shmuelof L, Zohary E (2005) Dissociation between ventral and dorsal fMRI activation during object and action recognition. Neuron 47(3):457–470
Shoval S, Borenstein J, Koren Y (1998) Auditory guidance with the navbelt-a computerized travel aid for the blind. IEEE Trans Syst Man Cybern Appl Rev 28(3):459–467
Spence C (2014) The skin as a medium for sensory substitution. Multisensory Res 27(5–6):293–312
Spiers HJ, Maguire EA (2006) Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31(4):1826–1840
Spiers HJ, Maguire EA (2007) Decoding human brain activity during real-world experiences. Trends Cogn Sci 11(8):356–365
Stoll C, Palluel-Germain R, Fristot V, Pellerin D, Alleysson D, Graff C (2015) Navigating from a depth image converted into sound. Appl Bionics Biomech 2015
Striem-Amit E, Amedi A (2014) Visual cortex extrastriate body-selective area activation in congenitally blind people “seeing” by using sounds. Curr Biol 24(6):687–692
Striem-Amit E, Cohen L, Dehaene S, Amedi A (2012a) Reading with sounds: sensory substitution selectively activates the visual word form area in the blind. Neuron 76(3):640–652
Striem-Amit E, Dakwar O, Hertz U, Meijer P, Stern W, Pascual-Leone A, Amedi A (2011) The neural network of sensory-substitution object shape recognition. Funct Neurol Rehab Ergon 1(2):271
Striem-Amit E, Dakwar O, Reich L, Amedi A (2012b) The large-scale organization of “visual” streams emerges without visual experience. Cereb Cortex 22(7):1698–1709
Striem-Amit E, Guendelman M, Amedi A (2012c) ‘Visual’acuity of the congenitally blind using visual-to-auditory sensory substitution. PLoS ONE 7(3):e33136
Striem-Amit E, Ovadia-Caro S, Caramazza A, Margulies DS, Villringer A, Amedi A (2015) Functional connectivity of visual cortex in the blind follows retinotopic organization principles. Brain 138(6):1679–1695
Sánchez J, Lumbreras M (1999) Virtual environment interaction through 3D audio by blind children. CyberPsychology Behav 2(2):101–111
Sánchez J, de la Torre N (2010) Autonomous navigation through the city for the blind. In: Proceedings of the 12th international ACM SIGACCESS conference on computers and accessibility (ASSETS’10). ACM Press, New York, p 195
Tan HM, Bassett JP, O’Keefe J, Cacucci F, Wills TJ (2015) The development of the head direction system before eye opening in the rat. Curr Biol 25(4):479–483
Tanaka K (1997) Mechanisms of visual object recognition: monkey and human studies. Curr Opin Neurobiol 7(4):523–529
Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207
Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10(2):436–447
Tcheang L, Bülthoff HH, Burgess N (2011) Visual influence on path integration in darkness indicates a multimodal representation of large-scale space. Proc Natl Acad Sci 108(3):1152–1157
Tinti C, Adenzato M, Tamietto M, Cornoldi C (2006) Visual experience is not necessary for efficient survey spatial cognition: evidence from blindness. Q J Exp Psychol 59(7):1306–1328
Tyler CW (2005) Varieties of synesthetic experience. In: Robertson LC, Sagiv N (eds)
Ungar S, Blades M, Spencer C (1993) The role of tactile maps in mobility training. Brit J Vis Impair 11(2):59–61
Ungar S, Blades M, Spencer C, Morsley K (1996) The ability of visually impaired children to locate themselves on a tactile map. J Vis Impair Blindness 90:526–535
Ungar S (2000) Cognitive mapping without vision. Cogn Map Past Present Future 4:221
Vercillo T, Burr D, Gori M (2016) Early visual deprivation severely compromises the auditory sense of space in congenitally blind children. Dev Psychol 52(6):847
Viard A, Doeller CF, Hartley T, Bird CM, Burgess N (2011) Anterior hippocampus and goal-directed spatial decision making. J Neurosci 31(12):4613–4621
Visell Y (2009) Tactile sensory substitution: Models for enaction in HCI. Interact Comput 21(1–2):38–53
Voss P, Lassonde M, Gougoux F, Fortin M, Guillemot JP, Lepore F (2004) Early-and late-onset blind individuals show supra-normal auditory abilities in far-space. Curr Biol 14(19):1734–1738
Voss P, Tabry V, Zatorre RJ (2015) Trade-off in the sound localization abilities of early blind individuals between the horizontal and vertical planes. J Neurosci 35(15):6051–6056
Voss P, Zatorre RJ (2011) Occipital cortical thickness predicts performance on pitch and musical tasks in blind individuals. Cereb Cortex bhr311
Vuillerme N, Hlavackova P, Franco C, Diot B, Demongeot J, Payan Y (2011) Can an electro-tactile vestibular substitution system improve balance in patients with unilateral vestibular loss under altered somatosensory conditions from the foot and ankle?. In: 2011 annual international conference of the IEEE Engineering in Medicine and Biology Society. IEEE, pp 1323–1326
Ward J, Meijer P (2010) Visual experiences in the blind induced by an auditory sensory substitution device. Conscious Cogn 19(1):492–500
Ward J, Wright T (2014) Sensory substitution as an artificially acquired synaesthesia. Neurosci Biobehav Rev 41:26–35
Whishaw IQ, Mittleman G, Bunch ST, Dunnett SB (1987) Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats. Behav Brain Res 24(2):125–138
White NM, McDonald RJ (2002) Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77(2):125–184
White BW, Saunders FA, Scadden L, Bach-Y-Rita P, Collins CC (1970) Seeing with the skin. Percept Psychophys 7(1):23–27
Wiener, S. I., & Taube, J. S. (2005). Head direction cells and the neural mechanisms of spatial orientation (bradford books). The MIT Press
Wolbers T, Klatzky RL, Loomis JM, Wutte MG, Giudice NA (2011) Modality-independent coding of spatial layout in the human brain. Curr Biol 21(11):984–989
Wolbers T, Wiener JM, Mallot HA, Büchel C (2007) Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. J Neurosci 27(35):9408–9416
Wolbers T, Hegarty M (2010) What determines our navigational abilities? Trends Cogn Sci 14:138–146
Zamm A, Schlaug G, Eagleman DM, Loui P (2013) Pathways to seeing music: Enhanced structural connectivity in colored-music synesthesia. NeuroImage 74:359–366
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG
About this chapter
Cite this chapter
Chebat, DR., Harrar, V., Kupers, R., Maidenbaum, S., Amedi, A., Ptito, M. (2018). Sensory Substitution and the Neural Correlates of Navigation in Blindness. In: Pissaloux, E., Velazquez, R. (eds) Mobility of Visually Impaired People. Springer, Cham. https://doi.org/10.1007/978-3-319-54446-5_6
Download citation
DOI: https://doi.org/10.1007/978-3-319-54446-5_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-54444-1
Online ISBN: 978-3-319-54446-5
eBook Packages: EngineeringEngineering (R0)