Animal Cognition

, Volume 17, Issue 3, pp 681–687 | Cite as

Dissociation of visual localization and visual detection in rhesus monkeys (Macaca mulatta)

  • Lau M. Andersen
  • Benjamin M. Basile
  • Robert R. Hampton
Original Paper

Abstract

Conscious and unconscious cognitive processes contribute independently to human behavior and can be dissociated. For example, humans report failing to see objects clearly in the periphery while simultaneously being able to grasp those objects accurately (Milner in Proc R Soc B Biol Sci 279:2289–2298, 2012). Knowing whether similar dissociations are present in nonverbal species is critical to our understanding of comparative psychology and the evolution of brains. However, such dissociations are difficult to detect in nonhumans because verbal reports of experience are the main way we discriminate putative conscious from unconscious processing. We trained monkeys in a localization task in which they responded to the location where a target appeared, and a matched detection task in which they reported the presence or absence of the same target. We used masking to manipulate the visibility of targets. Accuracy was high in both tasks when stimuli were unmasked and was attenuated by visual masking. At the strongest level of masking, performance in the detection task was at chance, while localization remained significantly above chance. Critically, errors in the detection task were predominantly misses, indicating that the monkeys’ behavior remained under stimulus control, but that the monkeys did not detect the target despite above-chance localization. While these results cannot establish the existence of phenomenal vision in monkeys, the dissociation of visually guided action from detection parallels the dissociation of conscious and unconscious vision seen in humans.

Keywords

Blindsight Masking Signal detection Perception Vision 

Supplementary material

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Supplementary material 1 (XLS 9 kb)
10071_2013_699_MOESM2_ESM.xls (10 kb)
Supplementary material 2 (XLS 10 kb)

References

  1. Breitmeyer BG, Öğmen H (2006) Visual masking: time slices through conscious and unconscious vision. Oxford University Press, OxfordCrossRefGoogle Scholar
  2. Cowey A, Stoerig P (1995) Blindsight in monkeys. Nature 373:247–249PubMedCrossRefGoogle Scholar
  3. Cowey A, Stoerig P (1997) Visual detection in monkeys with blindsight. Neuropsychologia 35:929–939PubMedCrossRefGoogle Scholar
  4. Dehaene S, Naccache L, Le Clec’H G, Koechlin E, Mueller M, Dehaene-Lambertz G, van de Moortele PF, Le Bihan D (1998) Imaging unconscious semantic priming. Nature 395:597–600PubMedCrossRefGoogle Scholar
  5. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222PubMedCrossRefGoogle Scholar
  6. Engel C, Singer W (2008) Better than conscious? Decision making, the human mind, and implications for institutions. MIT Press, CambridgeGoogle Scholar
  7. Fahrenfort JJ, Scholte HS, Lamme VAF (2007) Masking disrupts reentrant processing in human visual cortex. J Cogn Neurosci 19:1488–1497PubMedCrossRefGoogle Scholar
  8. Fehrer E, Raab D (1962) Reaction time to stimuli masked by metacontrast. J Exp Psychol 63:143–147PubMedCrossRefGoogle Scholar
  9. Francis G (1997) Cortical dynamics of lateral inhibition: metacontrast masking. Psychol Rev 104:572–594PubMedCrossRefGoogle Scholar
  10. Goodale M, Milner D (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25PubMedCrossRefGoogle Scholar
  11. Goodale AM, Milner AD (2004) Sight unseen: an exploration of conscious and unconscious vision. Oxford University Press, OxfordGoogle Scholar
  12. Goodale MA, Murphy K (1997) Action and perception in the visual periphery. In: Thier P, Karnath H-O (eds) Parietal lobe contributions to orientation in 3D space. Springer, Heidelberg, pp 447–461CrossRefGoogle Scholar
  13. Hannula DE, Simons DJ, Cohen NJ (2005) Imaging implicit perception: promise and pitfalls. Nat Rev Neurosci 6:247–255PubMedCrossRefGoogle Scholar
  14. Klotz W, Neumann O (1999) Motor activation without conscious discrimination in metacontrast masking. J Exp Psychol Hum Percept Perform 25:976–992CrossRefGoogle Scholar
  15. Kovács G, Vogels R, Orban GA (1995) Cortical correlate of pattern backward masking. Proc Natl Acad Sci 92:5587–5591PubMedCentralPubMedCrossRefGoogle Scholar
  16. Lamme VAF, Zipser K, Spekreijse H (2002) Masking interrupts figure-ground signals in V1. J Cogn Neurosci 14:1044–1053PubMedCrossRefGoogle Scholar
  17. Leopold DA (2012) Primary visual cortex: awareness and blindsight. Annu Rev Neurosci 35:91–109PubMedCentralPubMedCrossRefGoogle Scholar
  18. Macmillan NA, Creelman CD (2005) Detection theory: a user’s guide. Erlbaum, MahwahGoogle Scholar
  19. Milner AD (2012) Is visual processing in the dorsal stream accessible to consciousness? Proc R Soc B Biol Sci 279:2289–2298CrossRefGoogle Scholar
  20. Naccache L, Blandin E, Dehaene S (2002) Unconscious masked priming depends on temporal attention. Psychol Sci 13:416–424PubMedCrossRefGoogle Scholar
  21. Neumann O (1990) Direct parameter specification and the concept of perception. Psychol Res 52:207–215PubMedCrossRefGoogle Scholar
  22. Pisella L, Binkofski F, Lasek K, Toni I, Rossetti Y (2006) No double-dissociation between optic ataxia and visual agnosia: multiple sub-streams for multiple visuo-manual integrations. Neuropsychologia 44:2734–2748PubMedCrossRefGoogle Scholar
  23. van Gaal S, Ridderinkhof KR, Fahrenfort JJ, Scholte HS, Lamme VAF (2008) Frontal cortex mediates unconsciously triggered inhibitory control. J Neurosci 28:8053–8062PubMedCrossRefGoogle Scholar
  24. Weiskrantz L (1990) Blindsight: a case study and implications. Oxford University Press, OxfordCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Lau M. Andersen
    • 1
  • Benjamin M. Basile
    • 2
  • Robert R. Hampton
    • 2
  1. 1.Center for Functionally Integrative NeuroscienceAarhus UniversityAarhusDenmark
  2. 2.Emory UniversityAtlantaUSA

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