Nonvisual and Visual Object Shape Representations in Occipitotemporal Cortex: Evidence from Congenitally Blind and Sighted Adults

Knowledge of object shape is primarily acquired through the visual modality but can also be acquired through other sensory modalities. In the present study, we investigated the representation of object shape in humans without visual experience. Congenitally blind and sighted participants rated the shape similarity of pairs of 33 familiar objects, referred to by their names. The resulting shape similarity matrices were highly similar for the two groups, indicating that knowledge of the objects' shapes was largely independent of visual experience. Using fMRI, we tested for brain regions that represented object shape knowledge in blind and sighted participants. Multivoxel activity patterns were established for each of the 33 aurally presented object names. Sighted participants additionally viewed pictures of these objects. Using representational similarity analysis, neural similarity matrices were related to the behavioral shape similarity matrices. Results showed that activity patterns in occipitotemporal cortex (OTC) regions, including inferior temporal (IT) cortex and functionally defined object-selective cortex (OSC), reflected the behavioral shape similarity ratings in both blind and sighted groups, also when controlling for the objects' tactile and semantic similarity. Furthermore, neural similarity matrices of IT and OSC showed similarities across blind and sighted groups (within the auditory modality) and across modality (within the sighted group), but not across both modality and group (blind auditory–sighted visual). Together, these findings provide evidence that OTC not only represents objects visually (requiring visual experience) but also represents objects nonvisually, reflecting knowledge of object shape independently of the modality through which this knowledge was acquired.

[1]  J. G. Wallace,et al.  Recovery from early blindness : a case study , 1963 .

[2]  Alfonso Caramazza,et al.  The multiple semantics hypothesis: Multiple confusions? , 1990 .

[3]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

[5]  M. Kiyosawa,et al.  Auditory Triggered Mental Imagery of Shape Involves Visual Association Areas in Early Blind Humans , 2001, NeuroImage.

[6]  T. Hendler,et al.  Convergence of visual and tactile shape processing in the human lateral occipital complex. , 2002, Cerebral cortex.

[7]  Emiliano Ricciardi,et al.  Beyond sensory images: Object-based representation in the human ventral pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  William M. Stern,et al.  Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex , 2007, Nature Neuroscience.

[10]  Andrew D. Engell,et al.  Implicit Trustworthiness Decisions: Automatic Coding of Face Properties in the Human Amygdala , 2007, Journal of Cognitive Neuroscience.

[11]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[12]  Raymond J. Dolan,et al.  fMRI Activity Patterns in Human LOC Carry Information about Object Exemplars within Category , 2008, Journal of Cognitive Neuroscience.

[13]  Johan Wagemans,et al.  Perceived Shape Similarity among Unfamiliar Objects and the Organization of the Human Object Vision Pathway , 2008, The Journal of Neuroscience.

[14]  N. Kanwisher,et al.  Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity , 2008, PLoS biology.

[15]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[16]  J. Duncan,et al.  Top-Down Activation of Shape-Specific Population Codes in Visual Cortex during Mental Imagery , 2009, The Journal of Neuroscience.

[17]  G. Aguirre,et al.  Different spatial scales of shape similarity representation in lateral and ventral LOC. , 2009, Cerebral cortex.

[18]  A. Caramazza,et al.  Category-Specific Organization in the Human Brain Does Not Require Visual Experience , 2009, Neuron.

[19]  Thomas Serre,et al.  Reading the mind's eye: Decoding category information during mental imagery , 2010, NeuroImage.

[20]  Paul E. Downing,et al.  Unitary haptic perception: integrating moving tactile inputs from anatomically adjacent and non-adjacent digits , 2010, Experimental Brain Research.

[21]  R. Malach,et al.  Cortical activity during tactile exploration of objects in blind and sighted humans. , 2010, Restorative neurology and neuroscience.

[22]  Pawan Sinha,et al.  Corrigendum: The newly sighted fail to match seen with felt , 2011, Nature Neuroscience.

[23]  Radoslaw Martin Cichy,et al.  Imagery and perception share cortical representations of content and location. , 2012, Cerebral Cortex.

[24]  A. Caramazza,et al.  Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. , 2012, Journal of neurophysiology.

[25]  A. Caramazza,et al.  Conceptual Object Representations in Human Anterior Temporal Cortex , 2012, The Journal of Neuroscience.

[26]  Jennifer L. Milne,et al.  Shape-specific activation of occipital cortex in an early blind echolocation expert , 2013, Neuropsychologia.

[27]  Alfonso Caramazza,et al.  Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience , 2013, NeuroImage.

[28]  Alfonso Caramazza,et al.  Tool Selectivity in Left Occipitotemporal Cortex Develops without Vision , 2013, Journal of Cognitive Neuroscience.

[29]  R. Goebel,et al.  Human Object-Similarity Judgments Reflect and Transcend the Primate-IT Object Representation , 2013, Front. Psychol..