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Superadditive BOLD activation in superior temporal sulcus with threshold non-speech objects

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Abstract

Evidence from neurophysiological studies has shown the superior temporal sulcus (STS) to be a site of audio-visual integration, with neuronal response to audio-visual stimuli exceeding the sum of independent responses to unisensory audio and visual stimuli. However, experimenters have yet to elicit superadditive (AV > A+V) blood oxygen-level dependent (BOLD) activation from STS in humans using non-speech objects. Other studies have found integration in the BOLD signal with objects, but only using less stringent criteria to define integration. Using video clips and sounds of hand held tools presented at psychophysical threshold, we were able to elicit BOLD activation to audio-visual objects that surpassed the sum of the BOLD activations to audio and visual stimuli presented independently. Our findings suggest that the properties of the BOLD signal do not limit our ability to detect and define sites of integration using stringent criteria.

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References

  • Amedi A, von Kriegstein K, van Atteveldt NM, Beauchamp MS, Naumer MJ (2005) Functional imaging of human crossmodal identification and object recognition. Exp Brain Res 166:559–571

    Article  PubMed  CAS  Google Scholar 

  • Attwell D, Iadecola C (2002) The neural basis of functional brain imaging signals. Trends Neurosci 25:621–625

    Article  PubMed  CAS  Google Scholar 

  • Barraclough NE, Xiao D, Baker CI, Oram MW, Perret DI (2005) Integration of visual and auditory information by superior temporal sulcus neurons responsive to the sight of actions. J Cogn Neurosci 17:377–391

    Article  PubMed  Google Scholar 

  • Beauchamp MS (2005) Statistical criteria in fMRI studies od multisensory integration. Neuroinformatics 3:93–113

    Article  PubMed  Google Scholar 

  • Beauchamp MS, Argall BD, Bordurka J, Duyn JH, Martin A (2004a) Unraveling multisenory integration: patchy organization within human STS multisensory cortex. Nat Neurosci 7:1190–1192

    Article  CAS  Google Scholar 

  • Beauchamp MS, Lee KE, Argall BD, Martin A (2004b) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823

    Article  CAS  Google Scholar 

  • Benevento LA, Fallon J, Davis BJ, 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. Exp Neurol 57:849–872

    Article  PubMed  CAS  Google Scholar 

  • Binder JR, Frost JA, Hammeke TA, Bellgowan PSF, Rao SM, Cox RW (1999) Conceptual processing during the conscious resting state: a functional fMRI study. J Cogn Neurosci 11:80–93

    Article  PubMed  CAS  Google Scholar 

  • Birn RM, Cox RW, Bandettini PA (2002) Detection versus estimation in event-related fMRI: choosing the optimal stimulus timing. Neuroimage 15:252–264

    Article  PubMed  Google Scholar 

  • Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207–4221

    PubMed  CAS  Google Scholar 

  • Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    PubMed  CAS  Google Scholar 

  • Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 26:369–384

    Google Scholar 

  • Calvet GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex 11:1110–1123

    Article  Google Scholar 

  • Calvert GA, Campbell R, Brammer MJ (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Curr Biol 10:649–657

    Article  PubMed  CAS  Google Scholar 

  • Calvert GA, Hansen PC, Iversen SD, Brammer MJ (2001) Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect. Neuroimage 14:427–438

    Article  PubMed  CAS  Google Scholar 

  • Heeger DJ, Huk AC, Geisler WS, Albrecht AG (2000) Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 3:631–633

    Article  PubMed  CAS  Google Scholar 

  • Hershenson M (1962) Reaction time as a measure of intersensory facilitation. J Exp Psychol 63:289–293

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka K, Iwai E, Saito H, Tanaka K (1988) Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. J Neurophysiol 60:1615–1637

    PubMed  CAS  Google Scholar 

  • Laurienti PJ, Perrault TJ, Stanford TR, Wallace MT, Stein BE (2005) On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies. Exp Brain Res 166:289–297

    Article  PubMed  Google Scholar 

  • Logothetis NK (2002) The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 357:1003–1037

    Article  PubMed  Google Scholar 

  • Logothetis NK (2003) The underpinnings of the BOLD functional magnetic resonance inaging signal. J Neurosci 23:3963–3971

    PubMed  CAS  Google Scholar 

  • Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157

    Article  PubMed  CAS  Google Scholar 

  • Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769

    Article  PubMed  CAS  Google Scholar 

  • Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92:8135–8139

    Article  PubMed  CAS  Google Scholar 

  • Mateeff S, Hohnsbein J, Noack T (1985) Dynamic visual capture: apparent auditory motion induced by a moving visual target. Perception 14:721–727

    Article  PubMed  CAS  Google Scholar 

  • McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264:746–748

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA (2002) On the neuronal basis for multisensory convergence: a brief overview. Cogn Brain Res 14:31–40

    Article  Google Scholar 

  • Meredith MA, Nemitz JW, Stein BE (1987) Determinants of multisensory integration in the cat superior colliculus neurons I: temporal factors. J Neurosci 7:3215–3229

    PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1983) Interactions among converging sensory inputs in the superior colliculus. Science 221:389–391

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1986) Spatial factors determine the activity of multisensory neurons in cat superior colliculus. Brain Res 365:350–354

    Article  PubMed  CAS  Google Scholar 

  • Meredith MA, Stein BE (1996) Spatial determinates of multisensory integration in cat superior colliculus. J Neurophysiol 75:1843–1857

    PubMed  CAS  Google Scholar 

  • Morrell LK (1968) Temporal characteristics of sensory interaction in choice reaction times. J Exp Psychol 77:14–18

    Article  PubMed  CAS  Google Scholar 

  • Narain C, Scott SK, Wise RJ, Rosen S, Leff A, Iversen SD, Mathews PM (2003) Defining a left-lateralized response specific to intelligible speech using fMRI. Cereb Cortex 13:1362–1368

    Article  PubMed  CAS  Google Scholar 

  • Pelli DG (1997) The video toolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437–442

    PubMed  CAS  Google Scholar 

  • Perrault TJ Jr, Vaughn JW, Stein BE, Wallace MT (2005) Superior colliculus neurons use distinct operational modes in the integration of multisensory stimuli. J Neurophysiol 93:2575–2586

    Article  PubMed  Google Scholar 

  • Saxe R, Brett M, Kenwisher N (2006) Divide and conquer: a defense of functional localizers. Neuroimage 30:1088–1096

    Article  PubMed  Google Scholar 

  • Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex. Brain Res 149:1–24

    Article  PubMed  CAS  Google Scholar 

  • Semple MN, Scott SK (2003) Cortical mechanisms in hearing. Curr Opin Neurobiol 13:167–173

    Article  PubMed  CAS  Google Scholar 

  • Serences JT (2004) A comparison of methods for characterizing the event-related BOLD timeseries in rapid fMRI. Neuroimage 21:1690–1700

    Article  PubMed  Google Scholar 

  • Stanford TR, Quessy S, Stein BE (2005) Evaluating the operations underlying multisensory integration in the cat superior colliculus. J Neurosci 25:6499–6508

    Article  PubMed  CAS  Google Scholar 

  • Stark CE, Squire LR (2001) When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci USA 98:12760–12766

    Article  PubMed  CAS  Google Scholar 

  • Stein BE, Huneycutt WS, Meredith MA (1988) Neurons and behavior: the same rules of multisensory integration apply. Brain Res 448:355–358

    Article  PubMed  CAS  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, New York

    Google Scholar 

  • Ungeleider LG, Desimone R (1986) Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2. J Comp Neurol 248:147–163

    Article  Google Scholar 

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Acknowledgments

This research was supported in part by the Indiana METACyt Initiative of Indiana University, funded in part through a major grant from the Lilly Endowment, Inc. Thanks to Karin James and Laurel Stevenson, as well as James Townsend, Ami Eidels, and the Indiana University Neuroimaging Group for their insights on this work and manuscript.

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Authors and Affiliations

  1. Department of Psychological and Brain Sciences, Indiana University, 1101 East Tenth Street, Room 293, Bloomington, IN, 47405, USA

    Ryan A. Stevenson, Marisa L. Geoghegan & Thomas W. James

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  1. Ryan A. Stevenson
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  2. Marisa L. Geoghegan
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  3. Thomas W. James
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Correspondence to Ryan A. Stevenson.

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Stevenson, R.A., Geoghegan, M.L. & James, T.W. Superadditive BOLD activation in superior temporal sulcus with threshold non-speech objects. Exp Brain Res 179, 85–95 (2007). https://doi.org/10.1007/s00221-006-0770-6

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  • DOI: https://doi.org/10.1007/s00221-006-0770-6

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