Functional Preference for Object Sounds and Voices in the Brain of Early Blind and Sighted Individuals

Sounds activate occipital regions in early blind individuals. However, how different sound categories map onto specific regions of the occipital cortex remains a matter of debate. We used fMRI to characterize brain responses of early blind and sighted individuals to familiar object sounds, human voices, and their respective low-level control sounds. In addition, sighted participants were tested while viewing pictures of faces, objects, and phase-scrambled control pictures. In both early blind and sighted, a double dissociation was evidenced in bilateral auditory cortices between responses to voices and object sounds: Voices elicited categorical responses in bilateral superior temporal sulci, whereas object sounds elicited categorical responses along the lateral fissure bilaterally, including the primary auditory cortex and planum temporale. Outside the auditory regions, object sounds also elicited categorical responses in the left lateral and in the ventral occipitotemporal regions in both groups. These regions also showed response preference for images of objects in the sighted group, thus suggesting a functional specialization that is independent of sensory input and visual experience. Between-group comparisons revealed that, only in the blind group, categorical responses to object sounds extended more posteriorly into the occipital cortex. Functional connectivity analyses evidenced a selective increase in the functional coupling between these reorganized regions and regions of the ventral occipitotemporal cortex in the blind group. In contrast, vocal sounds did not elicit preferential responses in the occipital cortex in either group. Nevertheless, enhanced voice-selective connectivity between the left temporal voice area and the right fusiform gyrus were found in the blind group. Altogether, these findings suggest that, in the absence of developmental vision, separate auditory categories are not equipotent in driving selective auditory recruitment of occipitotemporal regions and highlight the presence of domain-selective constraints on the expression of cross-modal plasticity.

[1]  Amir Amedi,et al.  Origins of task-specific sensory-independent organization in the visual and auditory brain: neuroscience evidence, open questions and clinical implications , 2015, Current Opinion in Neurobiology.

[2]  Jochen Kaiser,et al.  Probing category selectivity for environmental sounds in the human auditory brain , 2008, Neuropsychologia.

[3]  P. Pietrini,et al.  New light from the dark: what blindness can teach us about brain function. , 2011, Current opinion in neurology.

[4]  Q. Gong,et al.  Transforming a left lateral fusiform region into VWFA through training in illiterate adults , 2010 .

[5]  R. Zatorre,et al.  Organization and Reorganization of Sensory-Deprived Cortex , 2012, Current Biology.

[6]  Tim Donovan,et al.  The Human Fetus Preferentially Engages with Face-like Visual Stimuli , 2017, Current Biology.

[7]  Bruno Rossion,et al.  Figures and figure supplements , 2014 .

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

[9]  N. Kanwisher Functional specificity in the human brain: A window into the functional architecture of the mind , 2010, Proceedings of the National Academy of Sciences.

[10]  Chunshui Yu,et al.  Thick Visual Cortex in the Early Blind , 2009, The Journal of Neuroscience.

[11]  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.

[12]  Simon Lacey,et al.  Object familiarity modulates the relationship between visual object imagery and haptic shape perception , 2010, NeuroImage.

[13]  Mark H. Johnson,et al.  Newborns' preferential tracking of face-like stimuli and its subsequent decline , 1991, Cognition.

[14]  Hanna Damasio,et al.  Naming the Same Entities from Visual or from Auditory Stimulation Engages Similar Regions of Left Inferotemporal Cortices , 2005, Journal of Cognitive Neuroscience.

[15]  R. Patterson,et al.  The Processing of Temporal Pitch and Melody Information in Auditory Cortex , 2002, Neuron.

[16]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[17]  C. Veraart,et al.  Functional Cerebral Reorganization for Auditory Spatial Processing and Auditory Substitution of Vision in Early Blind Subjects , 2006 .

[18]  G. Vandewalle,et al.  Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans , 2011, Proceedings of the National Academy of Sciences.

[19]  Katharina von Kriegstein,et al.  How do we recognise who is speaking? , 2014, Frontiers in bioscience.

[20]  M. Coltheart,et al.  Cognitive heterogeneity in genetically based prosopagnosia: a family study. , 2008, Journal of neuropsychology.

[21]  Denis Schluppeck,et al.  Neural responses to Mooney images reveal a modular representation of faces in human visual cortex , 2004, NeuroImage.

[22]  A. Cowey,et al.  Early Auditory Processing in Area V5/MT+ of the Congenitally Blind Brain , 2013, The Journal of Neuroscience.

[23]  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.

[24]  J. Rauschecker,et al.  A Positron Emission Tomographic Study of Auditory Localization in the Congenitally Blind , 2000, The Journal of Neuroscience.

[25]  J. Rauschecker,et al.  Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category , 2010, The Journal of Neuroscience.

[26]  William J. Talkington,et al.  Cortical network differences in the sighted versus early blind for recognition of human‐produced action sounds , 2011, Human brain mapping.

[27]  F. Lepore,et al.  Crossmodal plasticity in sensory loss. , 2011, Progress in brain research.

[28]  L. Cohen,et al.  A Ventral Visual Stream Reading Center Independent of Visual Experience , 2012, Current Biology.

[29]  R. Desimone Face-Selective Cells in the Temporal Cortex of Monkeys , 1991, Journal of Cognitive Neuroscience.

[30]  K. Nakayama,et al.  Human face recognition ability is specific and highly heritable , 2010, Proceedings of the National Academy of Sciences.

[31]  C. Büchel,et al.  Brain systems mediating voice identity processing in blind humans , 2014, Human brain mapping.

[32]  C. Blakemore,et al.  Tactile perception recruits functionally related visual areas in the late-blind , 2006, Neuroreport.

[33]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[34]  C. Carbon,et al.  Neural and genetic foundations of face recognition and prosopagnosia. , 2008, Journal of neuropsychology.

[35]  Aina Puce,et al.  Cortical Networks Representing Object Categories and High-level Attributes of Familiar Real-world Action Sounds , 2011, Journal of Cognitive Neuroscience.

[36]  Denise C. Park,et al.  Investigating Unique Environmental Contributions to the Neural Representation of Written Words: A Monozygotic Twin Study , 2012, PloS one.

[37]  Andreas Kleinschmidt,et al.  Interaction of Face and Voice Areas during Speaker Recognition , 2005, Journal of Cognitive Neuroscience.

[38]  Uta Noppeney,et al.  Prior auditory information shapes visual category-selectivity in ventral occipito-temporal cortex , 2010, NeuroImage.

[39]  R. Zatorre,et al.  Human temporal-lobe response to vocal sounds. , 2002, Brain research. Cognitive brain research.

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

[41]  Rebecca Saxe,et al.  Sensitive Period for a Multimodal Response in Human Visual Motion Area MT/MST , 2010, Current Biology.

[42]  Y. Yen,et al.  Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli , 2002, Journal of Cognitive Neuroscience.

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

[44]  H. Burton,et al.  Dissociating cortical regions activated by semantic and phonological tasks: a FMRI study in blind and sighted people. , 2003, Journal of neurophysiology.

[45]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[46]  G. Vandewalle,et al.  Impact of blindness onset on the functional organization and the connectivity of the occipital cortex. , 2013, Brain : a journal of neurology.

[47]  A. Caramazza,et al.  Object Domain and Modality in the Ventral Visual Pathway , 2016, Trends in Cognitive Sciences.

[48]  F. Gosselin,et al.  Audio-visual integration of emotion expression , 2008, Brain Research.

[49]  B. Rossion,et al.  Defining face perception areas in the human brain: A large-scale factorial fMRI face localizer analysis , 2012, Brain and Cognition.

[50]  R. Zatorre,et al.  Voice perception in blind persons: A functional magnetic resonance imaging study , 2009, Neuropsychologia.

[51]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[52]  J. Haxby,et al.  The effect of visual experience on the development of functional architecture in hMT+. , 2007, Cerebral cortex.

[53]  William J. Talkington,et al.  Human Cortical Organization for Processing Vocalizations Indicates Representation of Harmonic Structure as a Signal Attribute , 2009, The Journal of Neuroscience.

[54]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[55]  Alfred Anwander,et al.  Direct Structural Connections between Voice- and Face-Recognition Areas , 2011, The Journal of Neuroscience.

[56]  A. Caramazza,et al.  How Visual Is the Visual Cortex? Comparing Connectional and Functional Fingerprints between Congenitally Blind and Sighted Individuals , 2015, The Journal of Neuroscience.

[57]  Karl J. Friston,et al.  A multimodal language region in the ventral visual pathway , 1998, Nature.

[58]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[59]  Bruno L. Giordano,et al.  Abstract encoding of auditory objects in cortical activity patterns. , 2013, Cerebral cortex.

[60]  Javid Sadr,et al.  Object recognition and Random Image Structure Evolution , 2004, Cogn. Sci..

[61]  S. Crutch,et al.  Central auditory disorders: toward a neuropsychology of auditory objects. , 2010, Current opinion in neurology.

[62]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[63]  D. Bavelier,et al.  Cross-modal plasticity: where and how? , 2002, Nature Reviews Neuroscience.

[64]  M. Petrides The Human Cerebral Cortex: An MRI Atlas of the Sulci and Gyri in MNI Stereotaxic Space , 2011 .

[65]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

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

[67]  Manabu Honda,et al.  Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study , 2002, NeuroImage.

[68]  Tom Hartley,et al.  Selectivity for low-level features of objects in the human ventral stream , 2010, NeuroImage.

[69]  James W. Lewis,et al.  Auditory object salience: human cortical processing of non-biological action sounds and their acoustic signal attributes , 2012, Front. Syst. Neurosci..

[70]  M. Lassonde,et al.  Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects , 2008, Experimental Brain Research.

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

[72]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[73]  Timothy E. J. Behrens,et al.  Tools of the trade: psychophysiological interactions and functional connectivity. , 2012, Social cognitive and affective neuroscience.

[74]  Julie A. Brefczynski-Lewis,et al.  Auditory object perception: A neurobiological model and prospective review , 2017, Neuropsychologia.

[75]  Franco Lepore,et al.  Auditory motion in the sighted and blind: Early visual deprivation triggers a large-scale imbalance between auditory and “visual” brain regions , 2016, NeuroImage.

[76]  Bruno Rossion,et al.  Functional selectivity for face processing in the temporal voice area of early deaf individuals , 2017, Proceedings of the National Academy of Sciences.

[77]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[78]  K. Nakayama,et al.  Please Scroll down for Article Cognitive Neuropsychology Family Resemblance: Ten Family Members with Prosopagnosia and Within-class Object Agnosia , 2022 .

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

[80]  Leonid I. Perlovsky,et al.  Language and Cognition Interaction Neural Mechanisms , 2011, Comput. Intell. Neurosci..

[81]  T. Bourgeron,et al.  Genetic and Environmental Influences on the Visual Word Form and Fusiform Face Areas. , 2015, Cerebral cortex.

[82]  S. Scott,et al.  Retrieving meaning after temporal lobe infarction: The role of the basal language area , 2004, Annals of neurology.

[83]  Fuchun Lin,et al.  Progressive atrophy in the optic pathway and visual cortex of early blind Chinese adults: A voxel-based morphometry magnetic resonance imaging study , 2007, NeuroImage.

[84]  Y. Sugita Face perception in monkeys reared with no exposure to faces , 2008, Proceedings of the National Academy of Sciences.

[85]  Michael S. Beauchamp,et al.  Automatic Priming of Semantically Related Words Reduces Activity in the Fusiform Gyrus , 2005, Journal of Cognitive Neuroscience.

[86]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[87]  G. Yovel,et al.  A unified coding strategy for processing faces and voices , 2013, Trends in Cognitive Sciences.

[88]  Aina Puce,et al.  Different categories of living and non-living sound-sources activate distinct cortical networks , 2009, NeuroImage.

[89]  Emiliano Ricciardi,et al.  The blind brain: How (lack of) vision shapes the morphological and functional architecture of the human brain , 2014, Experimental biology and medicine.

[90]  O. Collignon,et al.  Functional selectivity in sensory-deprived cortices. , 2011, Journal of neurophysiology.

[91]  Denise C. Park,et al.  Nature versus Nurture in Ventral Visual Cortex: A Functional Magnetic Resonance Imaging Study of Twins , 2007, The Journal of Neuroscience.

[92]  F. Lepore,et al.  Plasticity of the Dorsal “Spatial” Stream in Visually Deprived Individuals , 2012, Neural plasticity.

[93]  A. Amedi,et al.  The brain as a flexible task machine: implications for visual rehabilitation using noninvasive vs. invasive approaches. , 2012, Current opinion in neurology.

[94]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[95]  Jeffrey R Binder,et al.  Human brain regions involved in recognizing environmental sounds. , 2004, Cerebral cortex.

[96]  Charles D. Smith,et al.  Dissociation of Automatic and Strategic Lexical-Semantics: Functional Magnetic Resonance Imaging Evidence for Differing Roles of Multiple Frontotemporal Regions , 2006, The Journal of Neuroscience.

[97]  Hartwig R. Siebner,et al.  The left fusiform gyrus hosts trisensory representations of manipulable objects , 2011, NeuroImage.

[98]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[99]  E. DeYoe,et al.  Distinct Cortical Pathways for Processing Tool versus Animal Sounds , 2005, The Journal of Neuroscience.

[100]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[101]  Jong Doo Lee,et al.  Morphological alterations in the congenital blind based on the analysis of cortical thickness and surface area , 2009, NeuroImage.

[102]  A. Caramazza,et al.  Brain Regions That Represent Amodal Conceptual Knowledge , 2013, The Journal of Neuroscience.

[103]  Karl J. Friston,et al.  Slice-timing effects and their correction in functional MRI , 2011, NeuroImage.

[104]  A. Nobre,et al.  Dissociating Linguistic Processes in the Left Inferior Frontal Cortex with Transcranial Magnetic Stimulation , 2022 .

[105]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[106]  F. Rösler,et al.  Speech processing activates visual cortex in congenitally blind humans , 2002, The European journal of neuroscience.

[107]  Karl J. Friston,et al.  Effects of visual deprivation on the organization of the semantic system. , 2003, Brain : a journal of neurology.