Abstract
This review surveys the recent literature on visuo-haptic convergence in the perception of object form, with particular reference to the lateral occipital complex (LOC) and the intraparietal sulcus (IPS) and discusses how visual imagery or multisensory representations might underlie this convergence. Drawing on a recent distinction between object- and spatially-based visual imagery, we propose a putative model in which LOtv, a subregion of LOC, contains a modality-independent representation of geometric shape that can be accessed either bottom-up from direct sensory inputs or top-down from frontoparietal regions. We suggest that such access is modulated by object familiarity: spatial imagery may be more important for unfamiliar objects and involve IPS foci in facilitating somatosensory inputs to the LOC; by contrast, object imagery may be more critical for familiar objects, being reflected in prefrontal drive to the LOC.
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References
Alivisatos B, Petrides M (1997) Functional activation of the human brain during mental rotation. Neuropsychologia 36:11–118
Amedi A, Malach R, Hendler T, Peled S, Zohary E (2001) Visuo-haptic object-related activation in the ventral visual pathway. Nat Neurosci 4:324–330
Amedi A, Jacobson G, Hendler T, Malach R, Zohary E (2002) Convergence of visual and tactile shape processing in the human lateral occipital complex. Cereb Cortex 12:1202–1212
Amedi A, Raz N, Pianka P, Malach R, Zohary E (2003) Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 6:758–766
Amedi A, Stern WM, Camprodon JA, Bermpohl F, Merabet L, Rotman S, Hemond C, Meijer P, Pascual-Leone A (2007) Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat Neurosci 10:687–689
Arno P, De Volder AG, Vanlierde A, Wanet-Defalque M-C, Streel E, Robert A, Sanabria-Bohórquez S, Veraart C (2001) Occipital activation by pattern recognition in the early blind using auditory substitution for vision. Neuroimage 13:632–645
Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P (2000) The functional anatomy of visual-tactile integration in man: a study using positron emission tomography. Neuropsychologia 38:115–124
Blajenkova O, Kozhevnikov M, Motes MA (2006) Object-spatial imagery: a new self-report imagery questionnaire. Appl Cognit Psychol 20:239–263
Burton H, Snyder AZ, Conturo TE, Akbudak E, Ollinger JM, Raichle ME (2002) Adaptive changes in early and late blind: a fMRI study of Braille reading. J Neurophysiol 87:589–607
Carpenter PA, Eisenberg P (1978) Mental rotation and the frame of reference in blind and sighted individuals. Percept Psychophys 23:117–124
De Volder AG, Toyama H, Kimura Y, Kiyosawa M, Nakano H, Vanlierde A, Wanet-Defalque M-C, Mishima M, Oda K, Ishiwata K, Senda M (2001) Auditory triggered mental imagery of shape involves visual association areas in early blind humans. Neuroimage 14:129–139
Dellantonio A, Spagnolo F (1990) Mental rotation of tactual stimuli. Acta Psychol 73:245–257
Deshpande G, Hu X, Stilla R, Sathian K (2008) Effective connectivity during haptic perception: a study using Granger causality analysis of functional magnetic resonance imaging data. Neuroimage 40:1807–1814
Easton RD, Greene AJ, Srinivas K (1997a) Transfer between vision and haptics: memory for 2-D patterns and 3-D objects. Psychon Bull Rev 4:403–410
Easton RD, Srinivas K, Greene AJ (1997b) Do vision and haptics share common representations? Implicit and explicit memory within and between modalities. J Exp Psychol Learn 23:153–163
Feinberg TE, Rothi LJ, Heilman KM (1986) Multimodal agnosia after unilateral left hemisphere lesion. Neurology 36:864–867
Gibson G, Stilla R, Sathian K (2008) Segregated visuo-haptic processing of texture and location. Abstract, Human Brain Mapping
Grefkes C, Fink G (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17
Grefkes C, Geyer S, Schormann T, Roland P, Zilles K (2001) Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. Neuroimage 14:617–631
Grefkes C, Weiss PH, Zilles K, Fink GR (2002) Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys. Neuron 35:173–184
Grefkes C, Ritzl A, Zilles K, Fink GR (2004) Human medial intraparietal cortex subserves visuomotor coordinate transformation. Neuroimage 23:1494–1506
Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10:14–23
Hadjikhani N, Roland PE (1998) Cross-modal transfer of information between the tactile and the visual representations in the human brain: a positron emission tomographic study. J Neurosci 18:1072–1084
Hollins M (1986) Haptic mental rotation: more consistent in blind subjects? J Visual Impair Blin 80:950–952
Iwamura Y (1998) Hierarchical somatosensory processing. Curr Opin Neurobiol 8:522–528
James TW, Humphrey GK, Gati JS, Servos P, Menon RS, Goodale MA (2002) Haptic study of three-dimensional objects activates extrastriate visual areas. Neuropsychologia 40:1706–1714
James TW, James KH, Humphrey GK, Goodale MA (2006) Do visual and tactile object representations share the same neural substrate? In: Heller MA, Ballesteros S (eds) Touch and blindness: psychology and neuroscience. Lawrence Erlbaum Associates, Mahwah, NJ, pp 139–155
Kosslyn SM (1973) Scanning visual images: some structural implications. Percept Psychophys 14:90–94
Kosslyn SM, Ball TM, Reiser BJ (1978) Visual images preserve metric spatial information: evidence from studies of image scanning. J Exp Psychol Human 4:47–60
Kourtzi Z, Kanwisher N (2000) Cortical regions involved in perceiving object shape. J Neurosci 20:3310–3318
Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293:1506–1509
Kourtzi Z, Tolias AS, Altmann CF, Augath M, Logothetis NK (2003) Integration of local features into global shapes: monkey and human fMRI studies. Neuron 37:333–346
Kozhevnikov M, Hegarty M, Mayer RE (2002) Revising the visualiser-verbaliser dimension: evidence for two types of visualisers. Cognit Instruct 20:47–77
Kozhevnikov M, Kosslyn SM, Shephard J (2005) Spatial versus object visualisers: a new characterisation of cognitive style. Mem Cognit 33:710–726
Krekelberg B, Boynton GM, van Wezel RJA (2006) Adaptation: from single cells to BOLD signals. Trends Neurosci 29:250–256
Lacey S, Campbell C (2006) Mental representation in visual/haptic crossmodal memory: evidence from interference effects. Q J Exp Psychol 59:361–376
Lacey S, Campbell C, Sathian K (2007a) Vision and touch: multiple or multisensory representations of objects? Perception 36:1513–1521
Lacey S, Peters A, Sathian K (2007b) Cross-modal object representation is viewpoint-independent. PLoS ONE 2:e890. doi:10.1371/journal.pone0000890
Large M-E, Aldcroft A, Vilis T (2007) Task-related laterality effects in the lateral occipital complex. Brain Res 1128:130–138
Lucan JN, Foxe JJ, Gomez-Ramirez M, Sathian K, Molholm S (2008) The spatio-temporal dynamics of somatosensory shape discrimination. Abstract, International Multisensory Research Forum
Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RBH (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92:8135–8139
Marmor GS, Zaback LA (1976) Mental rotation by the blind: does mental rotation depend on visual imagery? J Exp Psychol Human 2:515–521
Motes MA, Malach R, Kozhevnikov M (2008) Object-processing neural efficiency differentiates object from spatial visualizers. NeuroReport 19:1727–1731
Newman SD, Klatzky RL, Lederman SJ, Just MA (2005) Imagining material versus geometric properties of objects: an fMRI study. Cognit Brain Res 23:235–246
Pascual-Leone A, Hamilton RH (2001) The metamodal organization of the brain. Prog Brain Res 134:427–445
Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain. Annu Rev Neurosci 28:377–401
Peltier S, Stilla R, Mariola E, LaConte S, Hu X, Sathian K (2007) Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception. Neuropsychologia 45:476–483
Pietrini P, Furey ML, Ricciardi E, Gobbini MI, Wu W-HC, Cohen L, Guazzelli M, Haxby JV (2004) Beyond sensory images: object-based representation in the human ventral pathway. Proc Natl Acad Sci USA 101:5658–5663
Prather SC, Votaw JR, Sathian K (2004) Task-specific recruitment of dorsal and ventral visual areas during tactile perception. Neuropsychologia 42:1079–1087
Reales JM, Ballesteros S (1999) Implicit and explicit memory for visual and haptic objects: cross-modal priming depends on structural descriptions. J Exp Psychol Learn 25:644–663
Reed CL, Shoham S, Halgren E (2004) Neural substrates of tactile object recognition: an fMRI study. Hum Brain Mapp 21:236–246
Renier L, Collignon O, Tranduy D, Poirier C, Vanlierde A, Veraart C, De Volder A (2004) Visual cortex activation in early blind and sighted subjects using an auditory visual substitution device to perceive depth. Neuroimage 22:S1
Renier L, Collignon O, Poirier C, Tranduy D, Vanlierde A, Bol A, Veraart C, De Volder AG (2005) Cross modal activation of visual cortex during depth perception using auditory substitution of vision. Neuroimage 26:573–580
Röder B, Rösler F (1998) Visual input does not facilitate the scanning of spatial images. J Ment Imag 22:165–181
Saito DN, Okada T, Morita Y, Yonekura Y, Sadato N (2003) Tactile-visual cross-modal shape matching: a functional MRI study. Cognit Brain Res 17:14–25
Sathian K (2004) Modality, quo vadis?: comment. Behav Brain Sci 27:413–414
Sathian K (2005) Visual cortical activity during tactile perception in the sighted and the visually deprived. Dev Psychobiol 46:279–286
Sathian K, Lacey S (2007) Journeying beyond classical somatosensory cortex. Can J Exp Psychol 61:254–264
Sathian K, Zangaladze A, Hoffman JM, Grafton ST (1997) Feeling with the mind’s eye. Neuroreport 8:3877–3881
Shepard RN, Metzler J (1971) Mental rotation of three-dimensional objects. Science 171:701–703
Shikata E, McNamara A, Sprenger A, Hamzei F, Glauche V, Büchel C, Binkofski F (2008) Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks. Hum Brain Mapp 29:411–421
Stilla R, Sathian K (2008) Selective visuo-haptic processing of shape and texture. Hum Brain Mapp 29:1123–1138
Stilla R, Hanna R, Hu X, Mariola E, Deshpande G, Sathian K (2008a) Neural processing underlying tactile microspatial discrimination in the blind: a functional magnetic resonance imaging study. J Vis 8:1–19. doi:10.1167/8.10.13
Stilla R, Lacey S, Deshpande G, Hu X, Sathian K (2008b) Effective connectivity during haptic shape perception is modulated by object familiarity. Abstract, Society for Neuroscience
Stoesz M, Zhang M, Weisser VD, Prather SC, Mao H, Sathian K (2003) Neural networks active during tactile form perception: common and differential activity during macrospatial and microspatial tasks. Int J Psychophysiol 50:41–49
Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27:5326–5337
Tal N, Amedi A (2008) Using fMR-adaptation to study visual-tactile integration of objects in humans. Abstract, Israel Society for Neuroscience
Zhang M, Weisser VD, Stilla R, Prather SC, Sathian K (2004) Multisensory cortical processing of object shape and its relation to mental imagery. Cogn Affect Behav Ne 4:251–259
Zhou Y-D, Fuster JM (1997) Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task. Exp Brain Res 116:551–555
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This article is published as part of the Special Issue on Multisensory Integration.
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Lacey, S., Tal, N., Amedi, A. et al. A Putative Model of Multisensory Object Representation. Brain Topogr 21, 269–274 (2009). https://doi.org/10.1007/s10548-009-0087-4
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DOI: https://doi.org/10.1007/s10548-009-0087-4