Experimental Brain Research

, Volume 180, Issue 1, pp 153–161 | Cite as

A Bayesian model unifies multisensory spatial localization with the physiological properties of the superior colliculus

Research Article

Abstract

“Multisensory integration” refers to the phenomenon by which information from different senses is integrated in order to interpret and guide responses to external events. Here, we advance two specific hypotheses: (1) the process of multisensory integration in spatial localization is statistically optimal, and (2) the optimality of the processes guiding this localization results from the implementation of Bayes’ rule. We explicitly test the predictions of an optimal (Bayesian) model for the behavior of animals trained and tested in a spatial localization task, and find that the model correctly predicts behavioral patterns which are at times counterintuitive. The model also predicts the receptive field properties of superior colliculus neurons that are involved in these behaviors, and sheds new light on the computational responsibilities different circuits have in effecting these behaviors. Thus, the Bayesian model appears to represent not only a yardstick for the optimality of a behavior, but also a descriptor of the underlying neural processes.

References

  1. Alais D, Burr D (2004) The ventroliquist effect results from near-optimal bimodal integration. Curr Biol 14:257–262PubMedCrossRefGoogle Scholar
  2. Anastasio TJ, Patton PE (2004) Analysis and modeling of multisenosry enhancement in the deep superior colliculus. In: Calvert GA, Spence C, Stein BE (eds) The handbook of multisensory processes, Bradford Books/MIT, Cambridge, pp 265–284 Google Scholar
  3. Anastasio TJ, Patton PE, Belkacem-Boussaid K (2000) Using Bayes’ rule to model multisensory enhancement in the superior colliculus. Neural Comput 12:1165–1187PubMedCrossRefGoogle Scholar
  4. Battaglia PWJRA, Aslin RN (2003) Bayesian integration of visual and auditory signals for spatial localization. J Opt Soc Am A 20(7):1391–1397Google Scholar
  5. Beierholm UR, Quartz SR, Shams L (2005) Bayesian inference as a unifying model of auditory–visual integration and segregation. Program No. 283.13, Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC (Online)Google Scholar
  6. Casagrande VA, Harting JK, Hall WC, Diamond IT, Martin GF (1972) Superior colliculus of the tree shrew. A structural and functional subdivision into superficial and deep layers. Science 177:444–447PubMedCrossRefGoogle Scholar
  7. Colonius H, Diederich A (2004) Multisensory interaction in saccadic reaction time: a time-window-of-integration model. J Cogn Neurosci 16:1000–1009PubMedCrossRefGoogle Scholar
  8. Corneil BD, Munoz DP (1996) The influence of auditory and visual distractors on human orienting gaze shifts. J Neurosci 16:8193–8207PubMedGoogle Scholar
  9. Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415:429–433PubMedCrossRefGoogle Scholar
  10. Frassinetti F, Bolognini N, Ladavas E (2002) Enhancement of visual perception by crossmodal visuo-auditory interaction. Exp Brain Res 147:332–343PubMedCrossRefGoogle Scholar
  11. Frens MA, Van Opstal AJ, Van der Willigen RF (1995) Spatial and temporal factors determine auditory–visual interactions in human saccadic eye movements. Percept Psychophys 57:802–816PubMedGoogle Scholar
  12. Harris LR (1980) The superior colliculus and movements of the head and eyes in cats. J Physiol (Lond) 300:367–391Google Scholar
  13. Heffner RS, Heffner HE (1988) Sound localization acuity in the cat: effect of azimuth, signal duration, and test procedure. Hear Res 36:221–232PubMedCrossRefGoogle Scholar
  14. Hughes HC, Reuter-Lorenz PA, Nozawa G, Fendrich R (1994) Visual–auditory interactions in sensorimotor processing: saccades versus manual responses. J Exp Psychol Hum Percept Perform 20:131–153PubMedCrossRefGoogle Scholar
  15. Jiang W, Jiang H, Stein BE (2002) Two corticotectal areas facilitate multisensory orientation behavior. J Cogn Neurosci 14:1240–1255PubMedCrossRefGoogle Scholar
  16. Kadunce DC, Vaughan JW, Wallace MT, Benedek G, Stein BE (1997) Mechanisms of within- and cross-modality suppression in the superior colliculus2. J Neurophysiol 78:2834–2847PubMedGoogle Scholar
  17. Kadunce DC, Vaughan JW, Wallace MT, Stein BE (2001) The influence of visual and auditory receptive field organization on multisensory integration in the superior colliculus1. Exp Brain Res 139:303–310PubMedCrossRefGoogle Scholar
  18. Knill DC, Pouget A (2004) The Bayesian brain: the role of uncertainty in neural coding and computation. Trends Neurosci 27:712–719PubMedCrossRefGoogle Scholar
  19. May BJ, Huang AY (1996) Sound orientation behavior in cats. I. Localization of broadband noise. J Acoust Soc Am 100:1059–1069PubMedCrossRefGoogle Scholar
  20. Meredith MA, Stein BE (1983) Interactions among converging sensory inputs in the superior colliculus. Science 221:389–391PubMedCrossRefGoogle Scholar
  21. Meredith MA, Stein BE (1986) Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol 56:640–662PubMedGoogle Scholar
  22. Meredith MA, Stein BE (1996) Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75:1843–1857PubMedGoogle Scholar
  23. Middlebrooks JC (1987) Binaural mechanisms of spatial tuning in the cat’s superior colliculus distinguished using monaural occlusion. J Neurophysiol 57:688–701PubMedGoogle Scholar
  24. Middlebrooks JC, Knudsen EI (1984) A neural code for auditory space in the cat’s superior colliculus. J Neurosci 4:2621–2634PubMedGoogle Scholar
  25. Pavani F, Ladavas E, Driver J (2003) Auditory and multisensory aspects of visuospatial neglect. Trends Cogn Sci 7:407–414PubMedCrossRefGoogle Scholar
  26. Rauschecker JP, Kniepert U (1994) Auditory localization behaviour in visually deprived cats. Eur J Neurosci 6:149–160PubMedCrossRefGoogle Scholar
  27. Schneider GE (1969) Two visual systems: brain mechanisms for localization and discrimination are dissociated by tectal and cortical lesions. Science 163:895–902PubMedCrossRefGoogle Scholar
  28. Sparks DL (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol Rev 66:118–171PubMedGoogle Scholar
  29. Sprague JM (1965) The role of the superior colliculus in visually guided behavior42. Exp Neurol 11:115–146PubMedCrossRefGoogle Scholar
  30. Stein BE, Meredith MA (1993) The merging of the senses. MIT, CambridgeGoogle Scholar
  31. 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
  32. Wurtz RH, Albano JE (1980) Two visual systems: brain mechanisms for localization and discrimination are dissociated by tectal and cortical lesions. Annu Rev Neurosci 3:189–226PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Benjamin Rowland
    • 1
  • Terrence Stanford
    • 1
  • Barry Stein
    • 1
  1. 1.Wake Forest University School of Medicine, Neurobiology and AnatomyWinston-SalemUSA

Personalised recommendations