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Perception of complex motion in humans and pigeons (Columba livia)

Abstract

In the primate visual system, local motion signals are pooled to create a global motion percept. Like primates, many birds are highly dependent on vision for their survival, yet relatively little is known about motion perception in birds. We used random-dot stimuli to investigate pigeons’ ability to detect complex motion (radial, rotation, and spiral) compared to humans. Our human participants had a significantly lower threshold for rotational and radial motion when compared to spiral motion. The data from the pigeons, however, showed that the pigeons were most sensitive to rotational motion and least sensitive to radial motion, while sensitivity for spiral motion was intermediate. We followed up the pigeon results with an investigation of the effect of display aperture shape for rotational motion and velocity gradient for radial motion. We found no effect of shape of the aperture on thresholds, but did observe that radial motion containing accelerating dots improved thresholds. However, this improvement did not reach the thresholds levels observed for rotational motion. In sum, our experiments demonstrate that the pooling mechanism in the pigeon motion system is most efficient for rotation.

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References

  • Baron J, Pinto L, Dias MO, Lima B, Neuenschwander S (2007) Directional responses of visual wulst neurones to grating and plaid patterns in the awake owl. Eur J Neurosci 26:1950–1968

    PubMed  Article  Google Scholar 

  • Bischof WF, Reid SL, Wylie DR, Spetch ML (1999) Perception of coherent motion in random dot displays by pigeons and humans. Percept Psychophys 61:1089–1101

    CAS  PubMed  Article  Google Scholar 

  • Boussaoud D, Desimone R, Ungerleider LG (1992) Subcortical connections of visual areas MST and FST in macaques. Vis Neurosci 9:291–302

    CAS  PubMed  Article  Google Scholar 

  • Britten KJ, van Wezel RJ (1998) Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat Neurosci 1:59–63

    CAS  PubMed  Article  Google Scholar 

  • Burr DC, Thompson P (2011) Motion psychophysics: 1985–2010. Vis Res 51:1431–1456

    PubMed  Article  Google Scholar 

  • Burr DC, Badcock DR, Ross J (2001) Cardinal axes for radial and circular motion, revealed by summation and by masking. Vis Res 41:473–481

    CAS  PubMed  Article  Google Scholar 

  • Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation, 2nd edn. Wiley-Liss, New York

    Book  Google Scholar 

  • Chaves LM, Hodos W, Gunturkun O (1993) Color-reversal learning: effects after lesions of thalamic visual structures in pigeons. Vis Neurosci 10:1099–1107

    CAS  PubMed  Article  Google Scholar 

  • Crowder NA, Wylie DR (2001) Fast and slow neurons in the nucleus of the basal optic root in pigeons. Neurosci Lett 304:133–136

    CAS  PubMed  Article  Google Scholar 

  • Dakin SC, Bex PJ (2002) Summation of concentric orientation structure: seeing the Glass or the window? Vis Res 42:2013–2020

    CAS  PubMed  Article  Google Scholar 

  • Distler C, Hoffmann K-P (2001) Cortical input to the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN) in macaques: a retrograde tracing study. Cereb Cortex 11:572–580

    CAS  PubMed  Article  Google Scholar 

  • Duffy CJ, Wurtz RH (1991) Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J Neurophysiol 65:1329–1345

    CAS  PubMed  Google Scholar 

  • Edwards M, Badcock DR (1993) Asymmetries in the sensitivity to motion in depth: a centripetal bias. Perception 22:1013–1023

    CAS  PubMed  Article  Google Scholar 

  • Edwards M, Ibbotson MR (2007) Relative sensitivities to large-field optic-flow patterns varying in direction and speed. Perception 36:113–124

    PubMed  Article  Google Scholar 

  • Frost BJ (1985) Neural mechanisms for detecting object motion and figure–ground boundaries contrasted with self-motion detecting systems. In: Ingle D, Jeannerod M, Lee D (eds) Brain mechanisms and spatial vision. Nijhoff, Dordrecht, pp 415–419

    Chapter  Google Scholar 

  • Geesaman BJ, Andersen RA (1996) The analysis of complex motion patterns by form/cue invariant MSTd neurons. J Neurosci 16:4716–4732

    CAS  PubMed  Google Scholar 

  • Gibson JJ (1954) The visual perception of objective motion and subjective movement. Psychol Rev 64:304–314

    Article  Google Scholar 

  • Glass L (1969) Moire effect from random dots. Nature 223:578–580

    CAS  PubMed  Article  Google Scholar 

  • Graziano MS, Andersen RA, Snowden RJ (1994) Tuning of MST neurons to spiral motions. J Neurosci 14:54–67

    CAS  PubMed  Google Scholar 

  • Gu Y, Wang Y, Zhang T, Wang S-R (2002) Stimulus size selectivity and receptive field organization of ectostriatal neurons in the pigeon. J Comp Physiol A 188:173–178

    Article  Google Scholar 

  • Güntürkün O (2000) Sensory Physiology: Vision. In: Whittow GC (ed) Sturkie’s avian physiology. Academic Press, Orlando, pp 1–19

    Chapter  Google Scholar 

  • Hellmann B, Güntürkün O, Manns M (2004) Tectal mosaic: organization of the descending tectal projections in comparison to the ascending tectofugal pathway in the pigeon. J Comp Neurol 472:395–410

    PubMed  Article  Google Scholar 

  • Huk AC, Dougherty RF, Heeger DJ (2002) Retinotopy and functional subdivision of human areas MT and MST. J Neurosci 22:7195–7205

    CAS  PubMed  Google Scholar 

  • Husband S, Shimizu T (2001) Evolution of the avian visual system. In: Cook RG (ed) Avian visual cognition. www.pigeon.psy.tufts.edu/avc/husband/

  • Lazareva OF, Shimizu T, Wasserman EA (2012) How animals see the world: behavior, biology, and evolution of vision. Oxford University Press, London

    Book  Google Scholar 

  • Loidolt M, Aust U, Steurer M, Troje NF, Huber L (2006) Limits of dynamic object perception in pigeons: dynamic stimulus presentation does not enhance perception and discrimination of complex shape. Behaviour 34:71–85

    Google Scholar 

  • Maldonado PE, Maturana H, Varela DJ (1988) Frontal and lateral visual system in birds. Frontal and lateral gaze. Brain Behav Evol 32:57–62

    CAS  PubMed  Article  Google Scholar 

  • Martinoya C, Rivaud S, Bloch S (1983) Comparing frontal a n d lateral viewing in the pigeon. II. velocity thresholds for movement discrimination. Behav Brain Res 8:375–385

    CAS  PubMed  Article  Google Scholar 

  • May KA, Solomon JA (2013) Four theorems on the psychometric function. PLoS One 8(10):e74815

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Meese TS, Anderson SJ (2002) Spiral mechanisms are required to account for summation of complex motion components. Vis Res 42:1073–1080

    PubMed  Article  Google Scholar 

  • Meese TS, Harris MG (2001) Independent detectors for expansion and rotation, and for orthogonal components of deformation. Perception 30:1189–1202

    CAS  PubMed  Article  Google Scholar 

  • Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, Oxford

    Google Scholar 

  • Morrone MC, Burr DC, Di Pietro S, Stefanelli MA (1999) Cardinal directions for visual optic flow. Curr Biol 9:763–766

    CAS  PubMed  Article  Google Scholar 

  • Morrone MC, Tosetti M, Montanaro D, Fiorentini A, Cioni G, Burr DC (2000) A cortical area that responds specifically to optic flow, revealed by fMRI. Nat Neurosci 3:1322–1328

    CAS  PubMed  Article  Google Scholar 

  • Nakayama K (1985) Biological image motion processing: a review. Vis Res 25:625–660

    CAS  PubMed  Article  Google Scholar 

  • Nankoo J-F, Madan CR, Spetch ML, Wylie DR (2012) Perception of dynamic Glass patterns. Vis Res 72:55–62

    PubMed  Article  Google Scholar 

  • Nelder JA, Mead R (1965) A simplex method for function minimization. Comput J 7:308–313

    Article  Google Scholar 

  • Nguyen AP, Spetch ML, Crowder NA, Winship IR, Hurd PL, Wylie DRW (2004) A dissociation of motion and spatial-pattern vision in the avian telencephalon: implications for the evolution of “visual streams”. J Neurosci 24:4962–4970

    CAS  PubMed  Article  Google Scholar 

  • Nye PW (1973) On the functional differences between frontal and lateral visual fields of the pigeon. Vis Res 13:559–574

    CAS  PubMed  Article  Google Scholar 

  • Pelli DG, Farell B (1999) Why use noise? J Opt Soc Am A 16:647–653

    CAS  Article  Google Scholar 

  • Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Patria F, Galletti C (2010) Human V6: the medial motion area. Cereb Cortex 20:411–424

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Quick RF (1974) A vector-magnitude model of contrast detection. Kybernetik 16:65–67

    PubMed  Article  Google Scholar 

  • Rubene D, Håstad O, Tauson R, Wall H, Odeen A (2010) The presence of UV wavelengths improves the temporal resolution of the avian visual system. J Exp Biol 213:3357–3363

    PubMed  Article  Google Scholar 

  • Saito H, Yukie M, Tanaka K, Hikosaka K, Fukada Y, Iwai E (1986) Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. J Neurosci 6:145–157

    CAS  PubMed  Google Scholar 

  • Scase MO, Braddick OJ, Raymond JE (1996) What is noise for the motion system? Vis Res 36:2579–2586

    CAS  PubMed  Article  Google Scholar 

  • Shimizu T, Bowers AN (1999) Visual pathways in the avian telencephalon: evolutionary implications. Behav Brain Res 98:183–191

    CAS  PubMed  Article  Google Scholar 

  • Shimizu T, Patton TB, Husband S (2010) Avian visual behavior and the organization of the telencephalon. Brain Behav Evol 75:204–217

    PubMed Central  PubMed  Article  Google Scholar 

  • Shirai N, Kanazawa S, Yamaguchi MK (2006) Anisotropic motion coherence sensitivities to expansion/contraction motion in early infancy. Infant Child Dev 29:204–209

    Article  Google Scholar 

  • Simpson JI (1984) The accessory optic system. Annu Rev Neurosci 7:13–41

    CAS  PubMed  Article  Google Scholar 

  • Snowden RJ, Milne AB (1996) The effects of adapting to complex motions: position invariance and tuning to spiral motions. J Cogn Neurosci 8:435–452

    CAS  PubMed  Article  Google Scholar 

  • Tanaka K, Saito H (1989) Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. J Neurophysiol 62:626–641

    CAS  PubMed  Google Scholar 

  • Troje NF, Aust U (2013) What do you mean with “direction”? local and global cues to biological motion perception in pigeons. Vis Res 79:47–55

    PubMed  Article  Google Scholar 

  • Troje NF, Chang DHF (2013) Shape-independent processes in biological motion perception. In: Johnson KL, Shiffrar M (eds) People watching: social, perceptual, and neurophysiological studies of body perception. Oxford University Press, Oxford, pp 82–100

    Google Scholar 

  • Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT, Cambridge, pp 549–586

    Google Scholar 

  • Wall MB, Lingnau A, Ashida H, Smith AT (2008) Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation. Eur J Neurosci 27:2747–2757

    PubMed  Article  Google Scholar 

  • Wang YC, Jiang S, Frost BJ (1993) Visual processing in pigeon nucleus rotundus: luminance, color, motion, and looming subdivisions. Vis Neurosci 10:21–30

    CAS  PubMed  Article  Google Scholar 

  • Warren W (2004) Optic flow. In: Chalupa L, Werner J (eds) The visual neurosciences. MIT Press, Boston, pp 1391–1401

    Google Scholar 

  • Weibull W (1951) A statistical distribution function of wide applicability. J Appl Mech 18:292–297

    Google Scholar 

  • Wilson HR, Wilkinson F (1998) Detection of global structure in Glass patterns: Implications for form vision. Vis Res 38:2933–2947

    CAS  PubMed  Article  Google Scholar 

  • Wylie DR (2013) Processing of visual signals related to self-motion in the cerebellum of pigeons. Front Behav Neurosci 7:4

    PubMed Central  PubMed  Article  Google Scholar 

  • Wylie DRW, Crowder NA (2000) The spatiotemporal properties of fast and slow neurons in the pretectal lentiformis mesencephali in pigeons. J Neurophysiol 84:2529–2540

    CAS  PubMed  Google Scholar 

  • Wylie DR, Iwaniuk AN (2012) Neural mechanisms underlying visual motion detection in birds. In: Lazareva OF, Shimizu T, Wasserman EA (eds) How animals see the world: Behavior, biology, and evolution of vision. Oxford University Press, London, pp 289–318

    Chapter  Google Scholar 

  • Xiao Q, Frost BJ (2009) Looming responses of telencephalic neurons in the pigeon are modulated by optic flow. Brain Res 1035:40–46

    Article  Google Scholar 

  • Xiao Q, Li DP, Wang SR (2006) Looming-sensitive responses and receptive field organization of telencephalic neurons in the pigeon. Brain Res Bull 68:322–328

    PubMed  Article  Google Scholar 

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Acknowledgments

We would like to thank J.P., A.N.S. and M.K.M. for participating in our study. We would also like to thank Isaac Lank, Jeffrey Pisklak, and Jason Long for their help with technical issues and for running the pigeons in the experiments. This research was supported by grants from the National Science and Engineering Research Council (NSERC) of Canada to M.L.S. and D.R.W., and by an NSERC Alexander Graham Bell Canada Graduate Scholarship (Doctoral level) to C.R.M.

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Correspondence to Jean-François Nankoo.

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Nankoo, JF., Madan, C.R., Spetch, M.L. et al. Perception of complex motion in humans and pigeons (Columba livia). Exp Brain Res 232, 1843–1853 (2014). https://doi.org/10.1007/s00221-014-3876-2

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  • DOI: https://doi.org/10.1007/s00221-014-3876-2

Keywords

  • Visual perception
  • Motion perception
  • Columba livia
  • Coherence threshold
  • Motion integration