Skip to main content

Do rhesus monkeys (Macaca mulatta) perceive illusory motion?

Abstract

During the last decade, visual illusions have been used repeatedly to understand similarities and differences in visual perception of human and non-human animals. However, nearly all studies have focused only on illusions not related to motion perception, and to date, it is unknown whether non-human primates perceive any kind of motion illusion. In the present study, we investigated whether rhesus monkeys (Macaca mulatta) perceived one of the most popular motion illusions in humans, the Rotating Snake illusion (RSI). To this purpose, we set up four experiments. In Experiment 1, subjects initially were trained to discriminate static versus dynamic arrays. Once reaching the learning criterion, they underwent probe trials in which we presented the RSI and a control stimulus identical in overall configuration with the exception that the order of the luminance sequence was changed in a way that no apparent motion is perceived by humans. The overall performance of monkeys indicated that they spontaneously classified RSI as a dynamic array. Subsequently, we tested adult humans in the same task with the aim of directly comparing the performance of human and non-human primates (Experiment 2). In Experiment 3, we found that monkeys can be successfully trained to discriminate between the RSI and a control stimulus. Experiment 4 showed that a simple change in luminance sequence in the two arrays could not explain the performance reported in Experiment 3. These results suggest that some rhesus monkeys display a human-like perception of this motion illusion, raising the possibility that the neurocognitive systems underlying motion perception may be similar between human and non-human primates.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Agrillo C, Miletto Petrazzini ME, Dadda M (2013) Illusory patterns are fishy for fish, too. Front Neural Circuits 7:137. doi:10.3389/fncir.2013.00137

    PubMed Central  PubMed  Article  Google Scholar 

  2. Agrillo C, Parrish AE, Beran MJ (2014a) Do rhesus monkeys (Macaca mulatta) perceive the Zöllner illusion? Psychon Bull Rev 21(4):986–994

    PubMed  Article  Google Scholar 

  3. Agrillo C, Parrish AE, Beran MJ (2014b) Do primates see the solitaire illusion differently? A comparative assessment of humans (Homo sapiens), chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and capuchin monkeys (Cebus apella). J Comp Psych 128(4):402–413

    Article  Google Scholar 

  4. Ashida H, Kuriki I, Murakami I, Hisakata R, Kitaoka A (2012) Direction-specific fMRI adaptation reveals the visual cortical network underlying the ‘Rotating Snakes’ illusion. NeuroImage 61:1143–1152

    PubMed  Article  Google Scholar 

  5. Bååth R, Seno T, Kitaoka A (2014) Cats and illusory motion. Psychology. doi:10.4236/psych.2014.59125

    Google Scholar 

  6. Backus BT, Oruç İ (2005) Illusory motion from change over time in the response to contrast and luminance. J Vis 5(11):10

    Article  Google Scholar 

  7. Beer AL, Heckel AH, Greenlee MW (2008) A motion illusion reveals mechanisms of perceptual stabilization. PLoS ONE 3(7):e2741

    PubMed Central  PubMed  Article  Google Scholar 

  8. Beran MJ (2006) Quantity perception by adult humans (Homo sapiens), chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta) as a function of stimulus organization. Int J Comp Psych 19:386–397

    Google Scholar 

  9. Beran MJ, Parrish AE (2013) Visual nesting of stimuli affects rhesus monkeys’ (Macaca mulatta) quantity judgments in a bisection task. Atten Percept Psychophys 75:1243–1251

    PubMed Central  PubMed  Article  Google Scholar 

  10. Billino J, Hamburger K, Gegenfurtner KR (2009) Age effects on the perception of motion illusions. Perception 38:508

    PubMed  Article  Google Scholar 

  11. Burr D (2000) Are ‘speed lines’ used in human visual motion? Curr Biol 10(12):R440–R443

    CAS  PubMed  Article  Google Scholar 

  12. Conway BR, Kitaoka A, Yazdanbakhsh A, Pack CC, Livingstone MS (2005) Neural basis for a powerful static motion illusion. J Neurosci 25(23):5651–5656

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  13. Desimone R, Gross CG (1979) Visual areas in the temporal cortex of the macaque. Brain Res 178:363–380

    CAS  PubMed  Article  Google Scholar 

  14. Faubert J, Herbert AM (1999) The peripheral drift illusion: a motion illusion in the visual periphery. Perception 28(5):617–621

    CAS  PubMed  Article  Google Scholar 

  15. Fraser A, Wilcox KJ (1979) Perception of illusory movement. Nature 281:565–566

    CAS  PubMed  Article  Google Scholar 

  16. Fujita K, Blough DS, Blough PM (1991) Pigeons see the Ponzo illusion. Anim Learn Behav 19:283–293

    Article  Google Scholar 

  17. Fuss T, Bleckmann H, Schluessel V (2014) The brain creates illusions not just for us: sharks (Chiloscyllium griseum) can “see the magic” as well. Front Neural Circuits 8:24. doi:10.3389/fncir.2014.00024

    PubMed Central  PubMed  Article  Google Scholar 

  18. Gori S, Facoetti A (2014) Perceptual learning as a possible new approach for remediation and prevention of developmental dyslexia. Vis Res 99:78–87

    PubMed  Article  Google Scholar 

  19. Gori S, Hamburger K, Spillmann L (2006) Reversal of apparent rotation in the Enigma-figure with and without motion adaptation and the effect of T-junctions. Vis Res 46:3267–3273

    PubMed  Article  Google Scholar 

  20. Gori S, Pedersini R, Giora E (2008) How do painters represent motion in garments? Graphic invariants across centuries. Spat Vis 21:201–227

    PubMed  Article  Google Scholar 

  21. Gori S, Giora E, Stubbs DA (2010) Perceptual compromise between apparent and veridical motion indices: the Unchained-Dots illusion. Perception 39:863

    PubMed  Article  Google Scholar 

  22. Gori S, Giora E, Yazdanbakhsh A, Mingolla E (2011) A new motion illusion based on competition between two kinds of motion processing units: the Accordion grating. Neur Net 24:1082–1092

    Article  Google Scholar 

  23. Gori S, Agrillo C, Dadda M, Bisazza A (2014a) Do fish perceive illusory motion? Sci Rep 4:6443. doi:10.1038/srep06443

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. Gori S, Cecchini P, Bigoni A, Molteni M, Facoetti A (2014b) Magnocellular-dorsal pathway and sub-lexical route in developmental dyslexia. Front Hum Neurosci 8:460

    PubMed Central  PubMed  Article  Google Scholar 

  25. Gori S, Mascheretti S, Giora E, Ronconi L, Ruffino M, Quadrelli E, Facoetti A, Marino C (2014c) The DCDC2 intron 2 deletion impairs illusory motion perception unveiling the selective role of magnocellular-dorsal stream in reading (dis)ability. Cereb Cort. doi:10.1093/cercor/bhu234

    Google Scholar 

  26. Kitaoka A, Ashida H (2003) Phenomenal characteristics of the peripheral drift illusion. Vision 15:261–262

    Google Scholar 

  27. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920

    CAS  PubMed  Article  Google Scholar 

  28. Kuriki I, Ashida H, Murakami I, Kitaoka A (2008) Functional brain imaging of the Rotating Snakes illusion by fMRI. J Vis 8(16):11

    Article  Google Scholar 

  29. Murakami I, Kitaoka A, Ashida H (2006) A positive correlation between fixation instability and the strength of illusory motion in a static display. Vis Res 46:2421–2431

    PubMed  Article  Google Scholar 

  30. Nakamura N, Watanabe S, Fujita K (2008) Pigeons perceive the Ebbinghaus-Titchener circles as an assimilation illusion. J Exp Psychol Anim Behav Process 34:375–387

    PubMed  Article  Google Scholar 

  31. Naor-Raz G, Sekuler R (2000) Perceptual dimorphism in visual motion from stationary patterns. Perception 29(3):325–335

    CAS  PubMed  Google Scholar 

  32. Orban GA, Fize D, Peuskens H, Denys K, Nelissen K, Sunaert S, Todd J, Vanduffel W (2003) Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI. Neuropsychologia 41:1757–1768

    PubMed  Article  Google Scholar 

  33. Otero-Millan J, Macknik SL, Martinez-Conde S (2012) Microsaccades and blinks trigger illusory rotation in the “Rotating Snakes” illusion. J Neurosci 32:6043–6051

    CAS  PubMed  Article  Google Scholar 

  34. Parrish AE, Beran MJ (2014) When less is more: like humans, chimpanzees (Pan troglodytes) misperceive food amounts based on plate size. Anim Cogn 17:427–434

    PubMed Central  PubMed  Article  Google Scholar 

  35. Parron C, Fagot J (2007) Comparison of grouping abilities in humans (Homo sapiens) and baboons (Papio papio) with the Ebbinghaus illusion. J Comp Psychol 121:405–411

    PubMed  Article  Google Scholar 

  36. Petrov YA, Popple AV (2002) Effects of negative afterimages in visual illusions. J Opt Soc Am A 19(6):1107–1111

    Article  Google Scholar 

  37. Rees G, Friston K, Koch C (2000) A direct quantitative relationship between the functional properties of human and macaque V5. Nat Neurosci 3:716–723

    CAS  PubMed  Article  Google Scholar 

  38. Richardson WK, Washburn DA, Hopkins WD, Savage-Rumbaugh ES, Rumbaugh DM (1990) The NASA/LRC computerized test system. Behav Res Method Instrum Comput 22:127–131

    CAS  Article  Google Scholar 

  39. Ronconi L, Gori S, Ruffino M, Franceschini S, Urbani B, Molteni M, Facoetti A (2012) Decreased coherent motion discrimination in autism spectrum disorder: the role of attentional zoom-out deficit. PLoS ONE 7:e49019

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  40. Rosa Salva O, Rugani R, Cavazzana A, Regolin L, Vallortigara G (2013) Perception of the Ebbinghaus illusion in four-day-old domestic chicks (Gallus gallus). Anim Cogn 16:895–906

    CAS  PubMed  Article  Google Scholar 

  41. Ruzzoli M, Gori S, Pavan A, Pirulli C, Marzi CA, Miniussi C (2011) The neural basis of the Enigma illusion: a transcranial magnetic stimulation study. Neuropsychologia 49:3648–3655

    PubMed  Article  Google Scholar 

  42. Shimizu T, Bowers AN (1999) Visual circuits of the avian telencephalon: evolutionary implications. Behav Brain Res 98:183–191

    CAS  PubMed  Article  Google Scholar 

  43. Sovrano VA, Bisazza A (2009) Perception of subjective contours in fish. Perception 38:579–590

    PubMed  Article  Google Scholar 

  44. Sovrano VA, Albertazzi L, Rosa Salva O (2014) The Ebbinghaus illusion in a fish (Xenotoca eiseni). Anim Cogn 18(2):533–542

    PubMed  Article  Google Scholar 

  45. Spillmann L (2013) The Ouchi-Spillmann illusion revisited. Perception 42(4):413–429

    PubMed  Article  Google Scholar 

  46. Spinozzi G, De Lillo C, Truppa V (2003) Global and local processing of hierarchical visual stimuli in tufted capuchin monkeys (Cebus apella). J Comp Psychol 117:15–23

    PubMed  Article  Google Scholar 

  47. Stein J, Walsh V (1997) To see but not to read; the magnocellular theory of dyslexia. Trends Neurosci 20:147–152

    CAS  PubMed  Article  Google Scholar 

  48. Suganuma E, Pessoa V, Mongefuentes B, Castro B, Tavares M (2007) Perception of the Müller-Lyer illusion in capuchin monkeys (Cebus apella). Behav Brain Res 182:67–72

    PubMed  Article  Google Scholar 

  49. Tomimatsu E, Ito H, Sunaga S, Remijn GB (2011) Halt and recovery of illusory motion perception from peripherally viewed static images. Atten Percept Psychophys 73(6):1823–1832

    PubMed  Article  Google Scholar 

  50. Truppa V, Sovrano VA, Spinozzi G, Bisazza A (2010) Processing of visual hierarchical stimuli by fish (Xenotoca eiseni). Behav Brain Res 207:51–60

    PubMed  Article  Google Scholar 

  51. Watanabe S, Nakamura N, Fujita K (2013) Bantams (Gallus gallus domesticus) also perceive a reversed Zöllner illusion. Anim Cogn 16:109–115

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

This research was supported by FIRB Grant 2013 (RBFR13KHFS) from “Ministero dell’Istruzione, Università e Ricerca” (MIUR, Italy) to Christian Agrillo and by funding from the National Institutes of Health to Michael J. Beran (Grant HD-060563). The authors thank the three anonymous reviewers for their useful comments, Ted Evans and Audrey E. Parrish for assistance with data collection, and the Language Research Center staff for their care of the primates.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christian Agrillo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 2 (MP4 17958 kb)

Supplementary material 4 (MP4 22280 kb)

Supplementary material 1 (DOCX 10 kb)

Supplementary material 3 (BMP 2184 kb)

Supplementary material 5 (BMP 2397 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Agrillo, C., Gori, S. & Beran, M.J. Do rhesus monkeys (Macaca mulatta) perceive illusory motion?. Anim Cogn 18, 895–910 (2015). https://doi.org/10.1007/s10071-015-0860-6

Download citation

Keywords

  • Motion illusion
  • Rotating Snake illusion
  • Macaca mulatta
  • Comparative perception