Advertisement

Experimental Brain Research

, Volume 184, Issue 1, pp 39–52 | Cite as

Modality-specific selective attention attenuates multisensory integration

  • Jennifer L. Mozolic
  • Christina E. Hugenschmidt
  • Ann M. Peiffer
  • Paul J. Laurienti
Research Article

Abstract

Stimuli occurring in multiple sensory modalities that are temporally synchronous or spatially coincident can be integrated together to enhance perception. Additionally, the semantic content or meaning of a stimulus can influence cross-modal interactions, improving task performance when these stimuli convey semantically congruent or matching information, but impairing performance when they contain non-matching or distracting information. Attention is one mechanism that is known to alter processing of sensory stimuli by enhancing perception of task-relevant information and suppressing perception of task-irrelevant stimuli. It is not known, however, to what extent attention to a single sensory modality can minimize the impact of stimuli in the unattended sensory modality and reduce the integration of stimuli across multiple sensory modalities. Our hypothesis was that modality-specific selective attention would limit processing of stimuli in the unattended sensory modality, resulting in a reduction of performance enhancements produced by semantically matching multisensory stimuli, and a reduction in performance decrements produced by semantically non-matching multisensory stimuli. The results from two experiments utilizing a cued discrimination task demonstrate that selective attention to a single sensory modality prevents the integration of matching multisensory stimuli that is normally observed when attention is divided between sensory modalities. Attention did not reliably alter the amount of distraction caused by non-matching multisensory stimuli on this task; however, these findings highlight a critical role for modality-specific selective attention in modulating multisensory integration.

Keywords

Selective Attention Sensory Modality Divided Attention Race Model Multisensory Integration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank Ms Elizabeth Bennett for her assistance with data collection and analyses. This research was supported by NIH grant #NS042568.

References

  1. Alsius A, Navarra J, Campbell R, Soto-Faraco S (2005) Audiovisual integration of speech falters under high attention demands. Curr Biol 15:839–843PubMedCrossRefGoogle Scholar
  2. Bertelson P, Radeau M (1981) Cross-modal bias and perceptual fusion with auditory-visual spatial discordance. Percept Psychophys 29:578–584PubMedGoogle Scholar
  3. Bertelson P, Vroomen J, de Gelder B, Driver J (2000) The ventriloquist effect does not depend on the direction of deliberate visual attention. Percept Psychophys 62:321–332PubMedGoogle Scholar
  4. Burnett LR, Stein BE, Chaponis D, Wallace MT (2004) Superior colliculus lesions preferentially disrupt multisensory orientation. Neuroscience 124:535–547PubMedCrossRefGoogle Scholar
  5. Calvert GA, Campbell R, Brammer MJ (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Curr Biol 10:649–657PubMedCrossRefGoogle Scholar
  6. Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1990) Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248:1556–1559PubMedCrossRefGoogle Scholar
  7. Craik FI, Govoni R, Naveh-Benjamin M, Anderson ND (1996) The effects of divided attention on encoding and retrieval processes in human memory. J Exp Psychol Gen 125:159–180PubMedCrossRefGoogle Scholar
  8. Egner T, Hirsch J (2005) Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat Neurosci 8:1784–1790PubMedCrossRefGoogle Scholar
  9. Fan J, Flombaum JI, McCandliss BD, Thomas KM, Posner MI (2003) Cognitive and brain consequences of conflict. Neuroimage 18:42–57PubMedCrossRefGoogle Scholar
  10. Haxby JV, Horwitz B, Ungerleider LG, Maisog JM, Pietrini P, Grady CL (1994) The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J Neurosci 14:6336–6353PubMedGoogle Scholar
  11. Hershenson M (1962) Reaction time as a measure of intersensory facilitation. J Exp Psychol 63:289–293PubMedCrossRefGoogle Scholar
  12. Jiang W, Jiang H, Stein BE (2002) Two corticotectal areas facilitate multisensory orientation behavior. J Cogn Neurosci 14:1240–1255PubMedCrossRefGoogle Scholar
  13. Johnen A, Wagner H, Gaese BH (2001) Spatial attention modulates sound localization in barn owls. J Neurophysiol 85:1009–1012PubMedGoogle Scholar
  14. Johnson JA, Zatorre RJ (2005) Attention to simultaneous unrelated auditory and visual events: behavioral and neural correlates. Cereb Cortex 15:1609–1620PubMedCrossRefGoogle Scholar
  15. Johnson JA, Zatorre RJ (2006) Neural substrates for dividing and focusing attention between simultaneous auditory and visual events. Neuroimage 31:1673–1681PubMedCrossRefGoogle Scholar
  16. Kastner S, De Weerd P, Desimone R, Ungerleider LG (1998) Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282:108–111PubMedCrossRefGoogle Scholar
  17. Kawashima R, O’Sullivan BT, Roland PE (1995) Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the “mind’s eye”. Proc Natl Acad Sci USA 92:5969–5972PubMedCrossRefGoogle Scholar
  18. Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, Stein BE (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14:420–429PubMedCrossRefGoogle Scholar
  19. Laurienti PJ, Kraft RA, Maldjian JA, Burdette JH, Wallace MT (2004) Semantic congruence is a critical factor in multisensory behavioral performance. Exp Brain Res 158:405–414PubMedCrossRefGoogle Scholar
  20. Laurienti PJ, Burdette JH, Maldjian JA, Wallace MT (2006) Enhanced multisensory integration in older adults. Neurobiol Aging 27:1155–1163PubMedCrossRefGoogle Scholar
  21. Loose R, Kaufmann C, Auer DP, Lange KW (2003) Human prefrontal and sensory cortical activity during divided attention tasks. Hum Brain Mapp 18:249–259PubMedCrossRefGoogle Scholar
  22. Macaluso E, Frith CD, Driver J (2000) Modulation of human visual cortex by crossmodal spatial attention. Science 289:1206–1208PubMedCrossRefGoogle Scholar
  23. Macaluso E, Frith CD, Driver J (2002) Directing attention to locations and to sensory modalities: multiple levels of selective processing revealed with PET. Cereb Cortex 12:357–368PubMedCrossRefGoogle Scholar
  24. Macaluso E, George N, Dolan R, Spence C, Driver J (2004) Spatial and temporal factors during processing of audiovisual speech: a PET study. Neuroimage 21:725–732PubMedCrossRefGoogle Scholar
  25. McDonald JJ, Teder-Salejarvi WA, Di Russo F, Hillyard SA (2003) Neural substrates of perceptual enhancement by cross-modal spatial attention. J Cogn Neurosci 15:10–19PubMedCrossRefGoogle Scholar
  26. Miller J (1982) Divided attention: evidence for coactivation with redundant signals. Cognit Psychol 14:247–279PubMedCrossRefGoogle Scholar
  27. Miller J (1986) Timecourse of coactivation in bimodal divided attention. Percept Psychophys 40:331–343PubMedGoogle Scholar
  28. Moore CM, Egeth H (1998) How does feature-based attention affect visual processing? J Exp Psychol Hum Percept Perform 24:1296–1310PubMedCrossRefGoogle Scholar
  29. Morrell LK (1968) Temporal characteristics of sensory interaction in choice reaction times. J Exp Psychol 77:14–18PubMedCrossRefGoogle Scholar
  30. Motter BC (1993) Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol 70:909–919PubMedGoogle Scholar
  31. O’Leary DS, Andreasen NC, Hurtig RR, Torres IJ, Flashman LA, Kesler ML, Arndt SV, Cizadlo TJ, Ponto LLB, Watkins GL, Hichwa RD (1997) Auditory and visual attention assessed with PET. Hum Brain Mapp 5:422–436CrossRefGoogle Scholar
  32. Poliakoff E, Ashworth S, Lowe C, Spence C (2006) Vision and touch in ageing: crossmodal selective attention and visuotactile spatial interactions. Neuropsychologia 44:507–517PubMedCrossRefGoogle Scholar
  33. Posner MI, Driver J (1992) The neurobiology of selective attention. Curr Opin Neurobiol 2:165–169PubMedCrossRefGoogle Scholar
  34. Rees G, Frith C, Lavie N (2001) Processing of irrelevant visual motion during performance of an auditory attention task. Neuropsychologia 39:937–949PubMedCrossRefGoogle Scholar
  35. Reynolds JH, Chelazzi L, Desimone R (1999) Competitive mechanisms subserve attention in macaque areas V2 and V4. J Neurosci 19:1736–1753PubMedGoogle Scholar
  36. Shore DI, Simic N (2005) Integration of visual and tactile stimuli: top–down influences require time. Exp Brain Res 166:509–517PubMedCrossRefGoogle Scholar
  37. Spence C, Driver J (1997) On measuring selective attention to an expected sensory modality. Percept Psychophys 59:389–403PubMedGoogle Scholar
  38. Spence C, Nicholls ME, Gillespie N, Driver J (1998) Cross-modal links in exogenous covert spatial orienting between touch, audition, and vision. Percept Psychophys 60:544–557PubMedGoogle Scholar
  39. Spence C, Nicholls ME, Driver J (2001) The cost of expecting events in the wrong sensory modality. Percept Psychophys 63:330–336PubMedGoogle Scholar
  40. Spitzer H, Desimone R, Moran J (1988) Increased attention enhances both behavioral and neuronal performance. Science 240:338–340PubMedCrossRefGoogle Scholar
  41. Stein BE, Meredith MA, Huneycutt WS, McDade L (1989) Behavioral indices of multisensory integration: orientation to visual cues is affected by auditory stimuli. J Cogn Neurosci 1:12–24CrossRefGoogle Scholar
  42. Talsma D, Kok A (2001) Nonspatial intermodal selective attention is mediated by sensory brain areas: evidence from event-related potentials. Psychophysiology 38:736–751PubMedCrossRefGoogle Scholar
  43. Talsma D, Woldorff MG (2005) Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J Cogn Neurosci 17:1098–1114PubMedCrossRefGoogle Scholar
  44. Talsma D, Doty TJ, Woldorff MG (2007) Selective attention and audiovisual integration: is attending to both modalities a prerequisite for early integration? Cereb Cortex 17:679–690PubMedCrossRefGoogle Scholar
  45. Turatto M, Benso F, Galfano G, Umilta C (2002) Nonspatial attentional shifts between audition and vision. J Exp Psychol Hum Percept Perform 28:628–639PubMedCrossRefGoogle Scholar
  46. Turatto M, Galfano G, Bridgeman B, Umilta C (2004) Space-independent modality-driven attentional capture in auditory, tactile and visual systems. Exp Brain Res 155:301–310PubMedCrossRefGoogle Scholar
  47. Vroomen J, Bertelson P, de Gelder B (2001) The ventriloquist effect does not depend on the direction of automatic visual attention. Percept Psychophys 63:651–659PubMedGoogle Scholar
  48. Weissman DH, Giesbrecht B, Song AW, Mangun GR, Woldorff MG (2003) Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features. Neuroimage 19:1361–1368PubMedCrossRefGoogle Scholar
  49. Woodruff PW, Benson RR, Bandettini PA, Kwong KK, Howard RJ, Talavage T, Belliveau J, Rosen BR (1996) Modulation of auditory and visual cortex by selective attention is modality-dependent. Neuroreport 7:1909–1913PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Jennifer L. Mozolic
    • 1
    • 2
  • Christina E. Hugenschmidt
    • 1
    • 2
  • Ann M. Peiffer
    • 2
  • Paul J. Laurienti
    • 2
  1. 1.Graduate Program in NeuroscienceWake Forest University School of MedicineWinston-SalemUSA
  2. 2.ANSIR Laboratory, Department of RadiologyWake Forest University School of MedicineWinston-SalemUSA

Personalised recommendations