[en] Individuals who are deaf since early life may show enhanced performance at some visual tasks, including discrimination of directional motion. The neural substrates of such behavioral enhancements remain difficult to identify in humans, although neural plasticity has been shown for early deaf people in the auditory and association cortices, including the primary auditory cortex (PAC) and STS region, respectively. Here, we investigated whether neural responses in auditory and association cortices of early deaf individuals are reorganized to be sensitive to directional visual motion. To capture direction-selective responses, we recorded fMRI responses frequency-tagged to the 0.1-Hz presentation of central directional (100% coherent random dot) motion persisting for 2 sec contrasted with nondirectional (0% coherent) motion for 8 sec. We found direction-selective responses in the STS region in both deaf and hearing participants, but the extent of activation in the right STS region was 5.5 times larger for deaf participants. Minimal but significant direction-selective responses were also found in the PAC of deaf participants, both at the group level and in five of six individuals. In response to stimuli presented separately in the right and left visual fields, the relative activation across the right and left hemispheres was similar in both the PAC and STS region of deaf participants. Notably, the enhanced right-hemisphere activation could support the right visual field advantage reported previously in behavioral studies. Taken together, these results show that the reorganized auditory cortices of early deaf individuals are sensitive to directional motion. Speculatively, these results suggest that auditory and association regions can be remapped to support enhanced visual performance.
Disciplines :
Neurosciences & comportement
Auteur, co-auteur :
RETTER, Talia ; University of Nevada, Reno ; University of Louvain
Webster, Michael A; University of Nevada, Reno
Jiang, Fang; University of Nevada, Reno
Co-auteurs externes :
yes
Langue du document :
Anglais
Titre :
Directional Visual Motion Is Represented in the Auditory and Association Cortices of Early Deaf Individuals.
This research was supported by grants from the National Institutes of Health (NIH; grants EY023268 to F. J. and P20 GM103650 to M. A. W.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Talia L. Retter is supported by the Belgian National Foundation for Scientific Research (grant FC7159). The authors are thankful to Andrea Conte and Bruno Rossion for access to the stimulation program XPMan, Revision 111, as well as to Xiaoqing Gao for his help with the frequency domain analysis, and O. Scott Gwinn for use of his behavioral data on discrimination thresholds for the deaf participants as well as help with stimulus generation.
Albright, T. D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology, 52, 1106–1130.
Ales, J. M., & Norcia, A. M. (2009). Assessing direction-specific adaptation using the steady-state visual evoked potential: Results from EEG source imaging. Journal of Vision, 9, 8.
Allison, T., Puce, P., & McCarthy, G. (2000). Social perception from visual cues: Role of the STS region. Trends in Cognitive Sciences, 4, 267–278.
Almeida, J., He, D., Chen, Q., Mahon, B. Z., Zhang, F., Gonçalves, Ó. F., et al. (2015). Decoding visual location from neural patterns in the auditory cortex of the congenitally deaf. Psychological Science, 26, 1771–1782.
Anstis, S. M. (1970). Phi movement as a subtraction process. Vision Research, 10, 1411–1430.
Atkinson, J., Birtles, D., Anker, S., Braddick, O., Rutherford, M., Cowan, F., et al. (2008). High-density VEP measures of global form and motion processing in infants born very preterm. Journal of Vision, 8, 422.
Bandettini, P. A., Jesmanowicz, A., Wong, E. C., & Hyde, J. S. (1993). Processing strategies for time-course data sets in functional MRI of the human brain. Magnetic Resonance in Medicine, 30, 161–173.
Barnes, C. L., & Pandya, D. N. (1992). Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey. Journal of Comparative Neurology, 318, 222–244.
Baumgart, F., Gaschler-Markefski, B., Woldorff, M. G., Heinze, H. J., & Scheich, H. (1999). A movement-sensitive area in auditory cortex. Nature, 400, 724–726.
Bavelier, D., Brozinsky, C., Tomann, A., Mitchell, T., Neville, H., & Liu, G. (2001). Impact of early deafness and early exposure to sign language on the cerebral organization for motion processing. Journal of Neuroscience, 21, 8931–8942.
Bavelier, D., Dye, M. W. G., & Hauser, P. C. (2006). Do deaf individuals see better? Trends in Cognitive Sciences, 10, 512–518.
Bavelier, D., Tomann, A., Hutton, C., Mitchell, T., Corina, D., Liu, G., et al. (2000). Visual attention to the periphery is enhanced in congenitally deaf individuals. Journal of Neuroscience, 20, RC93.
Beauchamp, M. S., Argall, B. D., Bodurka, J., Duyn, J. H., & Martin, A. (2004). Unraveling multisensory integration: Patchy organization within human STS multisensory cortex. Nature Neuroscience, 7, 1190–1192.
Beauchamp, M. S., Cox, R. W., & DeYoe, E. A. (1997). Graded effects of spatial and featural attention on human area MT and associated motion processing areas. Journal of Neurophysiology, 78, 516–520.
Beauchamp, M. S., Yasar, N. E., Frye, R. E., & Ro, T. (2008). Touch, sound and vision in human superior temporal sulcus. Neuroimage, 41, 1011–1020.
Beckett, A., Peirce, J. W., Sanchez-Panchuelo, R. M., Francis, S., & Schluppeck, D. (2012). Contribution of large scale biases in decoding of direction-of-motion from high-resolution fMRI data in human early visual cortex. Neuroimage, 63, 1623–1632.
Benevento, L. A., Fallon, J., Davis, B. J., & Rezak, M. (1977). Auditory–visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey. Experimental Neurology, 57, 849–872.
Bola, L., Zimmermann, M., Mostowski, P., Jednorog, K., Marchewka, A., Butkowski, P., et al. (2017). Task-specific reorganization of the auditory cortex in deaf humans. Proceedings of the National Academy of Sciences, U.S.A., 114, E600–E609.
Bosworth, R. G., & Dobkins, K. R. (1999). Left-hemisphere dominance for motion processing in deaf signers. Psychological Science, 10, 256–262.
Bosworth, R. G., & Dobkins, K. R. (2002). Visual field asymmetries for motion processing in deaf and hearing signers. Brain and Cognition, 49, 170–181.
Bosworth, R. G., Petrich, J. A., & Dobkins, K. R. (2013). Effects of attention and laterality on motion and orientation discrimination in deaf signers. Brain and Cognition, 82, 117–126.
Bottari, D., Nava, E., Ley, P., & Pavani, F. (2010). Enhanced reactivity to visual stimuli in deaf individuals. Restorative Neurology and Neuroscience, 28, 167–179.
Braddick, O. (1974). A short-range process in apparent motion. Vision Research, 14, 519–527.
Braddick, O., Birtles, D., Wattam-Bell, J., & Atkinson, J. (2005). Motion-and orientation-specific cortical responses in infancy. Vision Research, 45, 3169–3179.
Braddick, O., Hartley, T., Atkinson, J., Wattam-Bell, J., & Turner, R. (1997). FMRI study of differential brain activation by coherent motion and dynamic noise. Investigative Ophthalmology & Visual Science, 38, 4297.
Braddick, O., Wattam-Bell, J., Birtles, D., Loesch, J., Loesch, L., Frazier, K., et al. (2008). Brain activity evoked by motion direction changes and by global motion coherence shows different spatial distributions. Journal of Vision, 8, 674.
Brandt, T., Stephan, T., Bense, S., Yousry, T. A., & Dieterich, M. (2000). Hemifield visual motion stimulation: An example of interhemispheric crosstalk. NeuroReport, 11, 2803–2809.
Brozinsky, C. J., & Bavelier, D. (2004). Motion velocity thresholds in deaf signers: Changes in lateralization but not in overall sensitivity. Cognitive Brain Research, 21, 1–10.
Bruce, C., Desimone, R., & Gross, C. G. (1981). Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. Journal of Neurophysiology, 46, 369–384.
Bulkin, D. A., & Groh, J. M. (2006). Seeing sounds: Visual and auditory interactions in the brain. Current Opinion in Neurobiology, 16, 415–419.
Calvert, G. A., Campbell, R., & Brammer, M. J. (2000). Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Current Biology, 10, 649–657.
Carlin, J. D., Rowe, J. B., Kriegeskorte, N., Thompson, R., & Calder, A. J. (2012). Direction-sensitive codes for observed head turns in human superior temporal sulcus. Cerebral Cortex, 22, 735–744.
Codina, C. J., Pascalis, O., Baseler, H. A., Levine, A. T., & Buckley, D. (2017). Peripheral visual reaction time is faster in deaf adults and British sign language interpreters than in hearing adults. Frontiers in Psychology, 8, 50.
Corballis, P. M. (2003). Visuospatial processing and the right-hemisphere interpreter. Brain and Cognition, 53, 171–176.
Dahl, C. D., Logothesis, N. K., & Kayser, C. (2009). Spatial organization of multisensory responses in temporal association cortex. Journal of Neuroscience, 29, 11924–11932.
Dubner, R., & Zeki, S. M. (1971). Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. Brain Research, 2, 528–532.
Ducommun, C. Y., Michel, C. M., Clarke, S., Adriani, M., Seeck, M., Landis, T., et al. (2004). Cortical motion deafness. Neuron, 43, 765–777.
Ducommun, C. Y., Murray, M. M., Thut, G., Bellmann, A., Viaud-Delmon, I., & Michel, C. M. (2002). Segregated processing of auditory motion and auditory location: An ERP mapping study. Neuroimage, 16, 76–88.
Dye, M. W. G., Hauser, P. C., & Bavelier, D. (2009). Is visual selective attention in deaf individuals enhanced or deficient? The case of the useful field of view. PLoS One, 4, e5640.
Eickhoff, S. B., Heim, S., Zeilles, K., & Amunts, K. (2006). Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage, 32, 570–582.
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage, 25, 1325–1335.
Engel, S., Zhang, X., & Wandell, B. (1997). Colour tuning in human visual cortex measured with functional magnetic resonance imaging. Nature, 388, 68–71.
Ernst, Z. R., Boynton, G. M., & Jazayeri, M. (2013). The spread of attention across features of a surface. Journal of Neurophysiology, 110, 2426–2439.
Felleman, D. J., & Van Essen, D. C. (1987). Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. Journal of Neurophysiology, 57, 889–920.
Fine, I., Finney, E. M., Boynton, G. M., & Dobkins, K. R. (2005). Comparing the effects of auditory deprivation and sign language within the auditory and visual cortex. Journal of Cognitive Neuroscience, 17, 1621–1637.
Finney, E. M., Clementz, B. A., Hickok, G., & Dobkins, K. R. (2003). Visual stimuli activate auditory cortex in deaf subjects: Evidence from MEG. NeuroReport, 14, 1425–1427.
Finney, E. M., Fine, I., & Dobkins, K. R. (2001). Visual stimuli activate auditory cortex in the deaf. Nature Neuroscience, 4, 1171–1173.
Gao, X., Gentile, F., & Rossion, B. (2017). Fast periodic stimulation (FPS): A highly effective approach in fMRI brain mapping. Brain Structure & Function, 223, 2433–2454.
Ghazanfar, A. A., & Schroeder, C. E. (2006). Is neocortex essentially multisensory? Trends in Cognitive Sciences, 10, 278–285.
Grossman, E. D., & Blake, R. (2001). Brain activity evoked by inverted and imagined biological motion. Vision Research, 41, 1475–1482.
Hackett, T. A., De La Mothe, L. A., Ulbert, I., Karmos, G., Smiley, J., & Schroeder, C. E. (2007). Multisensory convergence in auditory cortex: II. Thalamocortical connections of the caudal superior temporal plane. Journal of Comparative Neurology, 502, 924–952.
Hauthal, N., Sandmann, P., Debener, S., & Thorne, J. D. (2013). Visual movement perception in deaf and hearing individuals. Advances in Cognitive Psychology, 9, 53–61.
Hong, S. W., Tong, F., & Seiffert, A. E. (2013). Direction-selective patterns of activity in human visual cortex suggest common neural substrates for different types of motion. Neuropsychologia, 50, 514–521.
Hubel, D. H., & Wiesel, T. N. (1961). Integrative action in the cat’s lateral geniculate body. Journal of Physiology, 155, 385–398.
Huk, A. C., Ress, D., & Heeger, D. J. (2001). Neuronal basis of the motion aftereffect reconsidered. Neuron, 32, 161–172.
Jiang, F., Beauchamp, M. S., & Fine, I. (2015). Re-examining overlap between tactile and visual motion responses within hMT + and STS. Neuroimage, 119, 187–196.
Julesz, B. (1971). Foundations of cyclopean perception. Chicago: University of Chicago Press.
Kamitani, Y., & Tong, F. (2006). Decoding seen and attended motion directions from activity in the human visual cortex. Current Biology, 16, 1096–1102.
Karns, C. M., Dow, M. W., & Neville, H. J. (2012). Altered cross-modal processing in the primary auditory cortex of congenitally deaf adults: A visual-somatosensory fMRI study with a double-flash illusion. Journal of Neuroscience, 32, 9626–9638.
Koening-Robert, R., VanRullen, R., & Tsuchiya, N. (2015). Semantic wavelet-induced frequency-tagging (SWIFT) periodically activates category selective areas while steadily activating early visual areas. PLoS One, 10, e0144858.
Kubova, Z., Kuba, M., Hubacek, J., & Vit, F. (1990). Properties of visual evoked potentials to onset of movement on a television screen. Documenta Ophthalmologica, 75, 67–72.
Lam, K., Kaneoke, Y., Gunji, A., Yamasaki, H., Matsumoto, E., Naito, T., et al. (2000). Magnetic response of human extrastriate cortex in the detection of coherent and incoherent motion. Neuroscience, 97, 1–10.
Levine, A., Codina, C., Buckley, D., de Sousa, G., & Baseler, H. A. (2015). Differences in primary visual cortex predict performance in local motion detection in deaf and hearing adults. Journal of Vision, 15, 486.
Li, S. C. (2013). Neuromodulation and developmental contextual influences on neural and cognitive plasticity across the lifespan. Neuroscience & Biobehavioral Reviews, 37, 2201–2208.
Lomber, S. G., Meredith, M. A., & Kral, A. (2010). Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nature Neuroscience, 13, 1421–1427.
Lore, W. H., & Song, S. (1991). Central and peripheral visual processing in hearing and nonhearing individuals. Bulletin of the Psychonomic Society, 29, 437–440.
Meredith, M. A., Kryklywy, J., McMillan, A. J., Malhotra, S., Lum-Tai, R., & Lomber, S. G. (2011). Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex. Proceedings of the Natural Academy of Sciences, U.S.A., 108, 8856–8861.
Meyer, M., Baumann, S., Marchina, S., & Jancke, L. (2007). Hemodynamic responses in human multisensory and auditory association cortex to purely visual stimulation. BMC Neuroscience, 8, 14.
Mitchell, T. V., & Maslin, M. T. (2007). How vision matters for individuals with hearing loss. International Journal of Audiology, 46, 500–511.
Morosan, P., Rademacher, J., Schleicher, A., Amunts, K., Schomann, T., & Zilles, K. (2001). Human primary auditory cortex: Cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage, 13, 684–701.
Morrone, M. C., Tosetti, M., Montanaro, D., Fiorentini, A., Cioni, G., & Burr, D. C. (2000). A cortical area that responds specifically to optic flow, revealed by fMRI. Nature Neuroscience, 3, 1322–1328.
Motter, B. C., Steinmetz, M. A., Duffy, C. J., & Mountcastle, V. B. (1987). Functional properties of parietal visual neurons: Mechanisms of directionality along a single axis. Journal of Neuroscience, 7, 154–176.
Nakamura, H., Kashii, S., Naagamine, T., Hashimoto, T., Honda, Y., & Shibasaki, H. (2003). Human V5 demonstrated by magnetoencephalography using random dot kinematograms of different coherence levels. Neuroscience Research, 46, 423–433.
Nelissen, K., Vanduffel, W., & Orban, G. A. (2006). Charting the lower superior temporal region, a new motion-sensitive region in monkey superior temporal sulcus. Journal of Neuroscience, 26, 5929–5947.
Neville, H. J., Bavelier, D., Corina, D., Rauschecker, J., Karni, A., Lalwani, A., et al. (1998). Cerebral organization for language in deaf and hearing subjects: Biological constraints and effects of experience. Proceedings of the National Academy of Sciences, U.S.A., 95, 922–929.
Neville, H. J., & Lawson, D. (1987). Attention to central and peripheral visual space in a movement detection task: An event-related potential and behavioral study. II. Congenitally deaf adults. Brain Research, 405, 268–283.
Noguchi, Y., Kaneoke, Y., Kakigi, R., Tanabe, H. C., & Sadato, N. (2005). Role of the superior temporal region in human visual motion perception. Cerebral Cortex, 15, 1592–1601.
Oram, M. W., Perrett, D. I., & Hietanen, J. K. (1993). Directional tuning of motion-sensitive cells in the anterior superior temporal polysensory area of the macaque. Experimental Brain Research, 97, 274–294.
Palomares, M., Ales, J. M., Wade, A. R., Cottereau, B. R., & Norcia, A. M. (2012). Distinct effects of attention on the neural responses to form and motion processing: A SSVEP source-imaging study. Journal of Vision, 12, 15.
Parasnis, I. (1983). Effects of parental deafness and early exposure to manual communication on the cognitive skills, English language skill, and field independence of young deaf adults. Journal of Speech and Hearing Research, 26, 588–594.
Parasnis, I., & Samar, V. J. (1985). Parafoveal attention in congenitally deaf and hearing young adults. Brain and Cognition, 4, 313–327.
Pascual-Leone, A., & Hamilton, R. (2001). The metamodal organization of the brain. Progress in Brain Research, 134, 427–445.
Pavani, F., & Bottari, D. (2012). Visual abilities in individuals with profound deafness: A critical review. In M. M. Murray & M. T. Wallace (Eds.), The neural bases of multisensory processes. Boca Raton, FL: CRC Press/Taylor & Francis.
Puce, A., Allison, T., Gore, J. C., & McCarthy, G. (1995). Face-sensitive regions in human extrastriate cortex studied by functional MRI. Journal of Neurophysiology, 74, 1192–1199.
Retter, T. L., & Rossion, B. (2016). Uncovering the neural magnitude and spatio-temporal dynamics of natural image categorization in a fast visual stream. Neuropsychologia, 91, 9–28.
Sadato, N., Okada, T., Honda, M., Matsuki, K., Yoshida, M., Kashikura, K., et al. (2004). Cross-modal integration and plastic changes revealed by lip movement, random-dot motion and sign languages in the hearing and deaf. Cerebral Cortex, 15, 1113–1122.
Samar, V. J., & Parasnis, I. (2007). Non-verbal IQ is correlated with visual field advantages for short duration coherent motion detection in deaf signers with varied ASL exposure and etiologies of deafness. Brain and Cognition, 65, 260–269.
Sandmann, P., Dillier, N., Eichele, T., Meyer, M., Kegel, A., Pascual-Marqui, R. D., et al. (2012). Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users. Brain, 135, 555–568.
Saygin, A. P., & Sereno, M. I. (2008). Retinotopy and attention in human occipital, temporal, parietal, and frontal cortex. Cerebral Cortex, 18, 2158–2168.
Scott, G. D., Karns, C. M., Dow, M. W., Stevens, C., & Neville, H. J. (2014). Enhanced peripheral visual processing in congenitally deaf humans is supported by multiple brain regions, including primary auditory cortex. Frontiers in Human Neuroscience, 8, 177.
Seltzer, B., Cola, M. G., Gutierrez, C., Massee, M., Weldon, C., & Cusick, C. G. (1996). Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: Double anterograde tracer studies. Journal of Comparative Neurology, 370, 173–190.
Seltzer, B., & Pandya, D. N. (1978). Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research, 149, 1–24.
Seltzer, B., & Pandya, D. N. (1994). Parietal, temporal, and occipital projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study. Journal of Comparative Neurology, 343, 445–463.
Shiell, M. M., Champoux, F., & Zatorre, R. J. (2014). Enhancement of visual motion detection thresholds in early deaf people. PLoS One, 9, e90498.
Shiell, M. M., Champoux, F., & Zatorre, R. J. (2016). The right hemisphere planum temporale supports enhanced visual motion detection ability in deaf people: Evidence from cortical thickness. Neural Plasticity, 2016, 7217630.
Smiley, J. F., Hackett, T. A., Ulbert, I., Karmas, G., Lakatos, P., Javitt, D. C., et al. (2007). Multisensory convergence in auditory cortex: I. Cortical connections of the caudal superior temporal plane in macaque monkeys. Journal of Comparative Neurology, 502, 894–923.
Smith, K. R., Okada, K., Saberi, K., & Hickok, G. (2004). Human cortical auditory motion areas are not motion selective. NeuroReport, 15, 1523–1526.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
Tootell, R. B., Reppas, J. B., Dale, A. M., Look, R. B., Sereno, M. I., Malach, R., et al. (1995). Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature, 375, 139–141.
Tyler, C. W., & Kaitz, M. (1977). Movement adaptation in the visual evoked response. Experimental Brain Research, 27, 203–209.
Venezia, J. H., Vaden, K. I., Jr., Rong, F., Maddox, D., Saberi, K., & Hickok, G. (2017). Auditory, visual, and audiovisual speech processing streams in superior temporal sulcus. Frontiers in Human Neuroscience, 11, 174.
Wattam-Bell, J. (1991). Development of motion-specific cortical responses in infancy. Vision Research, 31, 287–297.
Weeks, R., Horwitz, B., Aziz-Sultan, A., Tian, B., Wessinger, C. M., Cohen, L. G., et al. (2000). A positron emission tomographic study of auditory localization in the congenitally blind. Journal of Neuroscience, 20, 2664–2672.
Zeki, S. M. (1978). Functional specialisation in the visual cortex of the rhesus monkey. Nature, 274, 423–428.
Zimmermann, J., Goebel, R., De Martino, F., van de Moortele, P. F., Feinberg, D., Adriany, G., et al. (2011). Mapping the organization of axis of motion selective features in human area MT using high-field fMRI. PLoS One, 6, e28716.
