Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-28T22:40:00.708Z Has data issue: false hasContentIssue false
  • English
  • Français

Multisensory integration substantiates distributed and overlapping neural networks

Published online by Cambridge University Press:  30 June 2016

Achille Pasqualotto
Achille Pasqualotto*
Affiliation:
Faculty of Arts and Social Sciences, Sabanci University, Tuzla 34956, Istanbul, Turkey. [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The hypothesis that highly overlapping networks underlie brain functions (neural reuse) is decisively supported by three decades of multisensory research. Multisensory areas process information from more than one sensory modality and therefore represent the best examples of neural reuse. Recent evidence of multisensory processing in primary visual cortices further indicates that neural reuse is a basic feature of the brain.

Type
Open Peer Commentary
Information
Behavioral and Brain Sciences , Volume 39 , 2016 , e127
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alain, C., Woods, D. L. & Knight, R. T. (1998) A distributed cortical network for auditory sensory memory in humans. Brain Research 812:23–37.Google Scholar
Amad, A., Cachia, A., Gorwood, P., Pins, D., Delmaire, C., Rolland, B., Mondino, M., Thomas, P. & Jardri, R. (2014) The multimodal connectivity of the hippocampal complex in auditory and visual hallucinations. Molecular Psychiatry 19:184–91.Google Scholar
Amedi, A., Raz, N., Pianka, P., Malach, R. & Zohary, E. (2003) Early “visual” cortex activation correlates with superior verbal memory performance in the blind. Nature Neuroscience 6:758–66.Google Scholar
Andersen, R. A., Essick, G. K. & Siegel, R. M. (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–58.CrossRefGoogle ScholarPubMed
Anderson, M. L. (2010) Neural reuse: A fundamental organizational principle of the brain. Behavioral and Brain Sciences 33(4):245–66. doi: 10.1017/S0140525X10000853.CrossRefGoogle ScholarPubMed
Anderson, M. L. (2014) After phrenology: Neural reuse and the interactive brain. MIT Press.Google Scholar
Bach-Y-Rita, P., Collins, C. C., Saunders, F. A., White, B. & Scadden, L. (1969) Vision substitution by tactile image projection. Nature 221:963–64.Google Scholar
Beauchamp, M. S. (2005) See me, hear me, touch me: Multisensory integration in lateral occipital-temporal cortex. Current Opinion in Neurobiology 15:145–53.CrossRefGoogle Scholar
Beauchamp, M. S., Yasar, N. E., Frye, R. E. & Ro, T. (2008) Touch, sound and vision in human superior temporal sulcus. NeuroImage 41:1011–20.Google Scholar
Beer, A. L., Plank, T. & Greenlee, M. W. (2011) Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex. Experimental Brain Research 213:299–308.Google Scholar
Beer, A. L., Plank, T., Meyer, G. & Greenlee, M. W. (2013) Combined diffusion-weighted and functional magnetic resonance imaging reveals a temporal-occipital network involved in auditory-visual object processing. Frontiers in Integrative Neuroscience 7:5.Google Scholar
Borra, E. & Rockland, K. S. (2011) Projections to early visual areas V1 and V2 in the calcarine fissure from parietal association areas in the macaque. Frontiers in Neuroanatomy 5:35.Google Scholar
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 46:369–84.Google Scholar
Burgess, N., Maguire, E. A., Spiers, H. J. & O'Keefe, J. (2001) A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. NeuroImage 14:439–53.Google Scholar
De Gelder, B. & Bertelson, P. (2003) Multisensory integration, perception and ecological validity. Trends in Cognitive Sciences 7:460–67.Google Scholar
Decharms, R. C. & Zador, A. (2000) Neural representation and the cortical code. Annual Review of Neuroscience 23:613–47.Google Scholar
Desgranges, B., Baron, J. C. & Eustache, F. (1998) The functional neuroanatomy of episodic memory: The role of the frontal lobes, the hippocampal formation, and other areas. NeuroImage 8:198–213.Google Scholar
Driver, J. & Noesselt, T. (2008) Multisensory interplay reveals crossmodal influences on “sensory-specific” brain regions, neural responses, and judgments. Neuron 57:11–23.Google Scholar
Duffau, H. (2008) The anatomo-functional connectivity of language revisited: New insights provided by electrostimulation and tractography. Neuropsychologia 46:927–34.CrossRefGoogle ScholarPubMed
Filippetti, M. L., Lloyd-Fox, S., Longo, M. R., Farroni, T. & Johnson, M. H. (2015) Neural mechanisms of body awareness in infants. Cerebral Cortex 25:3779–87.Google Scholar
Fuster, J. M. (1988) Prefrontal cortex. Birkhäuser.Google Scholar
Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. (1996) Action recognition in the premotor cortex. Brain 119:593–609.Google Scholar
Ganis, G., Thompson, W. L. & Kosslyn, S. M. (2004) Brain areas underlying visual mental imagery and visual perception: An fMRI study. Cognitive Brain Research 20:226–41.Google Scholar
Gauthier, I., Skudlarski, P., Gore, J. C. & Anderson, A. W. (2000) Expertise for cars and birds recruits brain areas involved in face recognition. Nature Neuroscience 3:191–97.Google Scholar
Gerstner, W., Kreiter, A. K., Markram, H. & Herz, A. V. (1997) Neural codes: Firing rates and beyond. Proceedings of the National Academy of Sciences 94:12740–41.Google Scholar
Gobbelé, R., Schürmann, M., Forss, N., Juottonen, K., Buchner, H. & Hari, R. (2003) Activation of the human posterior parietal and temporoparietal cortices during audiotactile interaction. NeuroImage 20:503–11.Google Scholar
Goldstein, E. (2009) Sensation and perception. Cengage Learning.Google Scholar
Grafton, S. T., Fadiga, L., Arbib, M. A. & Rizzolatti, G. (1997) Premotor cortex activation during observation and naming of familiar tools. NeuroImage 6:231–36.Google Scholar
Guerreiro, M. J., Putzar, L. & Röder, B. (2015) The effect of early visual deprivation on the neural bases of multisensory processing. Brain 138:1499–504.Google Scholar
Hagen, M. C., Franzén, O., McGlone, F., Essick, G., Dancer, C. & Pardo, J. V. (2002) Tactile motion activates the human middle temporal/V5 (MT/V5) complex. European Journal of Neuroscience 16:957–64.Google Scholar
Horwitz, B. & Braun, A. R. (2004) Brain network interactions in auditory, visual and linguistic processing. Brain and Language 89:377–84.Google Scholar
Iachini, T., Ruggiero, G. & Ruotolo, F. (2014) Does blindness affect egocentric and allocentric frames of reference in small and large scale spaces? Behavioural Brain Research 273:73–81.Google Scholar
Jiang, W., Wallace, M. T., Jiang, H., Vaughan, J. W. & Stein, B. E. (2001) Two cortical areas mediate multisensory integration in superior colliculus neurons. Journal of Neurophysiology 85:506–22.Google Scholar
Kauffman, T., Hamilton, R., Keenan, J. P., Warde, A. & Pascual-Leone, A. (2000) The role of visual cortex in tactile Braille reading: The early blind, the sighted, and the blindfolded. Annals of Neurology 48:418–19.Google Scholar
Kawachi, Y., Grove, P. M. & Sakurai, K. (2014) A single auditory tone alters the perception of multiple visual events. Journal of Vision 14:1–13.CrossRefGoogle ScholarPubMed
Kayser, C., Petkov, C. I. & Logothetis, N. K. (2008) Visual modulation of neurons in auditory cortex. Cerebral Cortex 18:1560–74.Google Scholar
Kim, M., Ducros, M., Carlson, T., Ronen, I., He, S., Ugurbil, K. & Kim, D.-S. (2006) Anatomical correlates of the functional organization in the human occipitotemporal cortex. Magnetic Resonance Imaging 24:583–90.Google Scholar
Lakatos, P., Chen, C. M., O'Connell, M. N., Mills, A. & Schroeder, C. E. (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–92.Google Scholar
Lawson, R., Boylan, A. & Edwards, L. (2014) Where you look can influence haptic object recognition. Attention, Perception, and Psychophysics 76:559–74.Google Scholar
Liang, M., Mouraux, A., Hu, L. & Iannetti, G. D. (2013) Primary sensory cortices contain distinguishable spatial patterns of activity for each sense. Nature Communications 4:1979.Google Scholar
Longo, M. R., Azañón, E. & Haggard, P. (2010) More than skin deep: Body representation beyond primary somatosensory cortex. Neuropsychologia 48:655–68.Google Scholar
Matsuhashi, M., Ikeda, A., Ohara, S., Matsumoto, R., Yamamoto, J., Takayama, M., Satowa, T., Begum, T., Usui, K., Nagamine, T., Mikuni, N., Takahashi, J., Miyamoto, S., Fukuyama, H. & Shibasaki, H. (2004) Multisensory convergence at human temporo-parietal junction – epicortical recording of evoked responses. Clinical Neurophysiology 115:1145–60.Google Scholar
Murray, M. M., Molholm, S., Michel, C. M., Heslenfeld, D. J., Ritter, W., Javitt, D. C., Schroeder, C. E. & Foxe, J. J. (2005) Grabbing your ear: Rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. Cerebral Cortex 15:963–74.CrossRefGoogle Scholar
Öngür, D. & Price, J. L. (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10:206–19.Google Scholar
Pascual-Leone, A. & Hamilton, R. (2001) The metamodal organization of the brain. Progress in Brain Research 134:427–45.Google Scholar
Pasqualotto, A., Finucane, C. M. & Newell, F. N. (2013a) Ambient visual information confers a context-specific, long-term benefit on memory for haptic scenes. Cognition 128:363–79.Google Scholar
Pasqualotto, A., Lam, J. S. Y. & Proulx, M. J. (2013b) Congenital blindness improves semantic and episodic memory. Behavioural Brain Research 244:162–65.Google Scholar
Pessoa, L. (2012) Beyond brain regions: Network perspective of cognition-emotion interactions. Behavioral and Brain Sciences 35:158–59.Google Scholar
Poirier, C., Collignon, O., Scheiber, C., Renier, L., Vanlierde, A., Tranduy, D., Veraart, C. & De Volder, A. G. (2006) Auditory motion perception activates visual motion areas in early blind subjects. NeuroImage 31:279–85.Google Scholar
Posner, M. I. & Rothbart, M. K. (2007) Research on attention networks as a model for the integration of psychological science. Annual Review of Psychology 58:1–23.Google Scholar
Proulx, M. J., Ptito, M. & Amedi, A. (2014) Multisensory integration, sensory substitution and visual rehabilitation. Neuroscience and Biobehavioral Reviews 41:1–2.CrossRefGoogle ScholarPubMed
Ravassard, P., Kees, A., Willers, B., Ho, D., Aharoni, D., Cushman, J., Aghajan, Z. M. & Mehta, M. R. (2013) Multisensory control of hippocampal spatiotemporal selectivity. Science 340:1342–46.Google Scholar
Ricciardi, E., Bonino, D., Pellegrini, S. & Pietrini, P. (2014) Mind the blind brain to understand the sighted one! Is there a supramodal cortical functional architecture? Neuroscience and Biobehavioral Reviews 41:64–77.Google Scholar
Rolls, E. T. & Tovee, M. J. (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. Journal of Neurophysiology 73:713–26.CrossRefGoogle ScholarPubMed
Sadato, N., Pascual-Leone, A., Grafman, J., Ibañez, V., Deiber, M.P., Dold, G. & Hallett, M. (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526–28.Google Scholar
Saenz, M., Lewis, L. B., Huth, A. G., Fine, I. & Koch, C. (2008) Visual motion area MT+/V5 responds to auditory motion in human sight-recovery subjects. Journal of Neuroscience 28:5141–48.Google Scholar
Sathian, K. & Zangaladze, A. (2002) Feeling with the mind's eye: Contribution of visual cortex to tactile perception. Behavioural Brain Research 135:127–32.Google Scholar
Sereno, M. I. & Huang, R. S. (2006) A human parietal face area contains aligned head-centered visual and tactile maps. Nature Neuroscience 9:1337–43.CrossRefGoogle ScholarPubMed
Serino, A., Canzoneri, E. & Avenanti, A. (2011) Fronto-parietal areas necessary for a multisensory representation of peripersonal space in humans: An rTMS study. Journal of Cognitive Neuroscience 23:2956–67.CrossRefGoogle ScholarPubMed
Shinkareva, S. V., Mason, R. A., Malave, V. L., Wang, W., Mitchell, T. M. & Just, M. A. (2008) Using fMRI brain activation to identify cognitive states associated with perception of tools and dwellings. PLoS One 3:e1394.Google Scholar
Shulman, G. L., Ollinger, J. M., Akbudak, E., Conturo, T. E., Snyder, A. Z., Petersen, S. E. & Corbetta, M. (1999) Areas involved in encoding and applying directional expectations to moving objects. Journal of Neuroscience 19:9480–96.Google Scholar
Stein, B. E., Huneycutt, W. S. & Meredith, M. A. (1988) Neurons and behavior: The same rules of multisensory integration apply. Brain Research 448: 355–58.Google Scholar
Stein, B. E. & Stanford, T. R. (2008) Multisensory integration: Current issues from the perspective of the single neuron. Nature Reviews Neuroscience 9:255–66.Google Scholar
Takahashi, T., Kansaku, K., Wada, M., Shibuya, S. & Kitazawa, S. (2013) Neural correlates of tactile temporal-order judgment in humans: An fMRI study. Cerebral Cortex 23:1952–64.Google Scholar
Uesaki, M. & Ashida, H. (2015) Optic-flow selective cortical sensory regions associated with self-reported states of vection. Frontiers in Psychology 6:775.Google Scholar
Vallar, G., Lobel, E., Galati, G., Berthoz, A., Pizzamiglio, L. & Le Bihan, D. (1999) A fronto-parietal system for computing the egocentric spatial frame of reference in humans. Experimental Brain Research 124:281–86.Google Scholar
Van Dijk, K. R. A., Hedden, T., Venkataraman, A., Evans, K. C., Lazar, S. W. & Buckner, R. L. (2010) Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. Journal of Neurophysiology 103:297–321.Google Scholar
Vidal, M. & Barrès, V. (2014) Hearing (rivalling) lips and seeing voices: How audiovisual interactions modulate perceptual stabilization in binocular rivalry. Frontiers in Human Neuroscience 8:677.Google Scholar
Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., Roffman, J. L., Smoller, J. W., Zollei, L., Polimeni, J. R., Fischl, B., Liu, H. & Buckner, R. L. (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology 106:1125–65.Google Scholar
Zangaladze, A., Epstein, C. M., Grafton, S. T. & Sathian, K. (1999) Involvement of visual cortex in tactile discrimination of orientation. Nature 401:587–90.Google Scholar