Enhancement of response times to bi- and tri-modal sensory stimuli during active movements

Research Article

Abstract

Simultaneous activation of two sensory modalities can improve perception and enhance performance. This multi-sensory enhancement had been previously observed only in conditions wherein participants were not performing any movement. Since tactile perception is attenuated during active movements, we investigated whether a bi- and a tri-modal enhancement can occur also when participants are presented with tactile stimuli, while engaged in active movements. Participants held a pen-like stylus and performed bidirectional writing-like movements inside a restricted workspace. During these movements participants were given a uni-modal sensory signal (visual––a thin gray line; auditory––a brief sound; haptic––a mechanical resisting force delivered through the stylus) or a bi- or tri-modal combination of these uni-modal signals, and their task was to respond, by pressing a button on the stylus, as soon as any one of these three stimuli was detected. Results showed that a combination of tri-modal signals was detected faster than any of the bi-modal combinations, which in turn were detected faster than any of the uni-modal signals. These facilitations exceeded the “Race model” predictions. A breakdown of the time gained in the bi-modal combinations by hemispace, hands and gender, provide further support for the “inverse effectiveness” principle, as the maximal bi-modal enhancements occurred for the least effective uni-modal responses.

Keywords

Multi-sensory enhancement Tri-modal Detection time Tactile attenuation Inverse effectiveness 

Notes

Acknowledgments

This research was funded by the EU research project PRESENCCIA––Presence: Research Encompassing Sensory Enhancement, Neuroscience, Cerebral-Computer Interfaces and Applications. We thank Mr. Gad Halevy for programming the computer for the experiment, and Ms. Ayelet Gal-Oz for her help in collecting the data. We also thank Mrs. Tatiana Gelfeld for her help in the race-model analysis.

References

  1. Angel RW, Malenka RC (1982) Velocity-dependent suppression of cutaneous sensitivity during movement. Exp Neurol 77(2):266–274PubMedCrossRefGoogle Scholar
  2. Bays PM, Wolpert DM (2007) Computational principles of sensorimotor control that minimize uncertainty and variability. J Physiol 278(2):387–396Google Scholar
  3. Bertelson P, Tisseyre F (1969) The time course of preparation: confirmatory results with visual and auditory warning signals. Acta Psychol 30:145–154CrossRefGoogle Scholar
  4. Boulinguez P, Ferrois M, Graumer G (2003). Hemispheric asymmetry for trajectory perception. Brain Res Cogn Brain Res 16(2):219–225PubMedCrossRefGoogle Scholar
  5. Chapman CE, Bushnell MC, Miron D, Duncan GH, Lund JP (1987) Sensory perception during movement in man. Exp Brain Res 68(3):516–524PubMedCrossRefGoogle Scholar
  6. Dalton P, Doolittle N, Nagata H, Breslin PA (2000) The merging of the senses: integration of subthreshold taste and smell. Nat Neurosci 3(5):431–432PubMedCrossRefGoogle Scholar
  7. Diederich A, Colonius H (1987) Intersensory facilitation in the motor component? Psychol Res 49(1):23–29CrossRefGoogle Scholar
  8. Diederich A, Colonius H (2004) Bimodal and trimodal multisensory enhancement: effects of stimulus onset and intensity on reaction time. Percept Psychophys 66(8):1388–1404PubMedGoogle Scholar
  9. Diederich A, Colonius H, Bockhorst D, Tabeling S (2003) Visual-tactile spatial interaction in saccade generation. Exp Brain Res 148(3):328–337PubMedGoogle Scholar
  10. Doyle MC, Snowden RJ (2001) Identification of visual stimuli is improved by accompanying auditory stimuli: the role of eye movements and sound location. Perception 30(7):795–810PubMedCrossRefGoogle Scholar
  11. Duysens J, Tax AA, Nawijn S, Berger W, Prokop T, Altenmuller E (1995) Gating of sensation and evoked potentials following foot stimulation during human gait. Exp Brain Res 105(3):423–431PubMedGoogle Scholar
  12. Forster B, Cavina-Pratesi C, Aglioti S, Berlucchi G (2002) Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time. Exp Brain Res 143(4):480–487PubMedCrossRefGoogle Scholar
  13. Fort A, Delpuech C, Pernier J, Giard MH (2002) Dynamics of cortico-subcortical cross-modal operations involved in audio-visual object detection in humans. Cereb Cortex 12(10):1031–1039PubMedCrossRefGoogle Scholar
  14. Frassinetti F, Bolognini N, Làdavas E (2002) Acoustic vision of neglected stimuli: interaction among spatially converging audiovisual inputs in neglect patients. J Cogn Neurosci 14(1):62–69PubMedCrossRefGoogle Scholar
  15. Frassinetti F, Bolognini N, Bottari D, Bonora A, Làdavas E, (2005) Audio-visual integration in patients with visual deficit. J Cogn Neurosci 17(9):1442–1452PubMedCrossRefGoogle Scholar
  16. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in Rhesus monkey auditory cortex. J Neurosci 25(20):5004–5012PubMedCrossRefGoogle Scholar
  17. Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11(5):473–490PubMedCrossRefGoogle Scholar
  18. Hershenson M (1962) Reaction time as a measure of intersensory facilitation. J Exp Psychol 63:289–293PubMedCrossRefGoogle Scholar
  19. Jiang W, Wallace MT, Jiang H, Vaughan JW, Stein BE (2001) Two cortical areas mediate multisensory integration in superior colliculus neurons. J Neurophysiol 85(2):506–522PubMedGoogle Scholar
  20. Kayser C, Petkov CI, Augath M, Logothetis NK (2005) Integration of touch and sound in auditory cortex. Neuron 48(2):373–384PubMedCrossRefGoogle Scholar
  21. Körding KP, Wolpert DM (2006) Bayesian decision theory in sensorimotor control. Trends Cogn Sci 10(7):320–326CrossRefGoogle Scholar
  22. Laurienti PJ, Burdette JH, Maldjian JA, Wallace MT (2006) Enhanced multisensory integration in older adults. Neurobiol Aging 27(8):1155–1163PubMedCrossRefGoogle Scholar
  23. Lovelace CT, Stein BE, Wallace MT (2003) An irrelevant light enhances auditory detection in humans: a psychophysical analysis of multisensory integration in stimulus detection. Brain Res Cogn Brain Res 17(2):447–453PubMedCrossRefGoogle Scholar
  24. Mergner T, Rosemeier T (1998) Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions: a conceptual model. Brain Res Brain Res Rev 28(1–2):118–135PubMedCrossRefGoogle Scholar
  25. Miller J (1982) Divided attention: evidence for coactivation with redundant signals. Cognit Psychol 14(2):247–279PubMedCrossRefGoogle Scholar
  26. Miller J (1986) Time course of coactivation in bimodal divided attention. Percept Psychophys 40:331–334PubMedGoogle Scholar
  27. Molholm S, Ritter W, Javitt DC, Foxe JJ (2004) Multisensory visual-auditory object recognition in humans: a high-density electrical mapping study. Cereb Cortex 14(4):452–465PubMedCrossRefGoogle Scholar
  28. Nickerson RS (1973) Intersensory facilitation of reaction time: energy summation or preparation enhancement?. Psychol Rev 80(6):489–509PubMedCrossRefGoogle Scholar
  29. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  30. Oliveri M, Rossini PM, Pasqualetti P, Traversa R, Cicinelli P, Palmieri MG, Tomaiuolo F, Caltagirone C (1999) Interhemispheric asymmetries in the perception of unimanual and bimanual cutaneous stimuli. Brain 122(9):1721–1729PubMedCrossRefGoogle Scholar
  31. Perrault TJ Jr, Vaughan JW, Stein BE, Wallace MT (2003) Neuron-specific response characteristics predict the magnitude of multisensory integration. J Neurophysiol 90(6):4022–4026PubMedCrossRefGoogle Scholar
  32. Posner MI, Klein R, Summers J, Buggie S (1973) On the selection of signals. Mem Cognit 1:2–12Google Scholar
  33. Post LJ, Zompa IC, Chapman CE (1994) Perception of vibrotactile stimuli during motor activity in human subjects. Exp Brain Res 100(1):107–120PubMedCrossRefGoogle Scholar
  34. Raab DH (1962) Statistical facilitation of simple reaction times. Trans N Y Acad Sci 24:574–590PubMedGoogle Scholar
  35. Rowland BA, Stanford TR, Stein BE (2007) A Bayesian model unifies multisensory spatial localization with the physiological properties of the superior colliculus. Exp Brain Res 180(1):153–161PubMedCrossRefGoogle Scholar
  36. Sanders AF (1980) Stage analysis of reaction process. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior. Amsterdam North Holland, pp 331–354Google Scholar
  37. Schmidt RF, Schady WJ, Torebjork HE (1990a) Gating of tactile input from the hand. I. Effects of finger movement. Exp Brain Res 79(1):97–102PubMedCrossRefGoogle Scholar
  38. Schmidt RF, Torebjork HE, Schady WJ (1990b) Gating of tactile input from the hand. II. Effects of remote movements and anaesthesia. Exp Brain Res 79(1):103–108PubMedGoogle Scholar
  39. Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316PubMedCrossRefGoogle Scholar
  40. Smith EE (1968) Choice reaction time: an analysis of major theoretical positions. Psychol Bull 69(2):77–110PubMedCrossRefGoogle Scholar
  41. Stein BE, London N, Wilkinson LK, Price DD (1996) Enhancement of perceived visual intensity by auditory stimuli: a psychophysical analysis. J Cogn Neurosci 8:497–506CrossRefGoogle Scholar
  42. Sumby WH, Pollack I (1954) Visual contribution to speech intelligibility in noise. J Acoust Soc Am 26:212–215CrossRefGoogle Scholar
  43. Todd JW (1912) Reaction to multiple stimuli. Arch Psychol (25):1–65Google Scholar
  44. Ulrich R, Miller J, Schröter H (2007) Testing the race model inequality: an algorithm and computer programs. Behav Res Methods Instr 39(2):291–302Google Scholar
  45. Voss M, Ingram JN, Haggard P, Wolpert DM (2005) Sensorimotor attenuation by central motor command signals in the absence of movement. Nat Neurosci 9:26–27PubMedCrossRefGoogle Scholar
  46. Wallace MT, Meredith MA, Stein BE (1998) Multisensory integration in the superior colliculus of the alert cat. J Neurophysiol 80(2):1006–1010PubMedGoogle Scholar
  47. Williams SR, Chapman CE (2000) Time course and magnitude of movement-related gating of tactile detection in humans. II. Effects of stimulus intensity on detection and scaling of tactile stimuli. J Neurophysiol 84(2):863–875PubMedGoogle Scholar
  48. Williams SR, Chapman CE (2002) Time course and magnitude of movement-related gating of tactile detection in humans. III. Effect of motor task. J Neurophysiol 88(4):1968–1979PubMedCrossRefGoogle Scholar
  49. Williams SR, Shenasa J, Chapman CE (1998) Time course and magnitude of movement-related gating of tactile detection in humans. I. Importance of stimulus location. J Neurophysiol 79(2):947–963PubMedGoogle Scholar
  50. Zellner DA, Kautz MA (1990) Color affects perceived odor intensity. J Exp Psychol Hum Percept Perform 16(2):391–397PubMedCrossRefGoogle Scholar
  51. Zellner DA, Bartoli AM Eckard R (1991) Influence of color on odor identification and liking ratings. Am J Psychol 104(4):547–561PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.The Touch Laboratory, Department of Education in Technology and ScienceTechnion - Israel Institute of TechnologyHaifaIsrael
  2. 2.The Brain-Behavior Research CenterUniversity of HaifaHaifaIsrael

Personalised recommendations