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Interactions between top-down and bottom-up attention in barn owls (Tyto alba)

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Abstract

Selective attention, the prioritization of behaviorally relevant stimuli for behavioral control, is commonly divided into two processes: bottom-up, stimulus-driven selection and top-down, task-driven selection. Here, we tested two barn owls in a visual search task that examines attentional capture of the top-down task by bottom-up mechanisms. We trained barn owls to search for a vertical Gabor patch embedded in a circular array of differently oriented Gabor distractors (top-down guided search). To track the point of gaze, a lightweight wireless video camera was mounted on the owl’s head. Three experiments were conducted in which the owls were tested in the following conditions: (1) five distractors; (2) nine distractors; (3) five distractors with one distractor surrounded by a red circle; or (4) five distractors with a brief sound at the initiation of the stimulus. Search times and number of head saccades to reach the target were measured and compared between the different conditions. It was found that search time and number of saccades to the target increased when the number of distractors was larger (condition 2) and when an additional irrelevant salient stimulus, auditory or visual, was added to the scene (conditions 3 and 4). These results demonstrate that in barn owls, bottom-up attention interacts with top-down attention to shape behavior in ways similar to human attentional capture. The findings suggest similar attentional principles in taxa that have been evolutionarily separated for 300 million years.

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References

  • Awh E, Belopolsky AV, Theeuwes J (2012) Top-down versus bottom-up attentional control: a failed theoretical dichotomy. Trends Cogn Sci 16:437–443

    Article  PubMed  PubMed Central  Google Scholar 

  • Ben-Tov M, Donchin O, Ben-Shahar O, Segev R (2015) Pop-out in visual search of moving targets in the archer fish. Nat Commun 6:6476

    Article  CAS  PubMed  Google Scholar 

  • Berti S (2013) The role of auditory transient and deviance processing in distraction of task performance: a combined behavioral and event-related brain potential study. Front Hum Neurosci 7:352

    Article  PubMed  PubMed Central  Google Scholar 

  • Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    Article  CAS  PubMed  Google Scholar 

  • Bushnell PJ, Strupp BJ (2009) Assessing attention in rodents. In: Buccafusco JJ (ed) Methods of behavior analysis in Neuroscience, 2nd edn. CRC Press, Boca Raton, FL

    Google Scholar 

  • Carrasco M, Yeshurun Y (1998) The contribution of covert attention to the set-size and eccentricity effects in visual search. J Exp Psychol Hum Percept Perform 24:673–692

    Article  CAS  PubMed  Google Scholar 

  • Cook RG, Cavoto KK, Cavoto BR (1996) Mechanisms of multidimensional grouping, fusion, and search in avian texture discrimination. Anim Learn Behav 24:150–167

    Article  Google Scholar 

  • Cook RG, Cavoto BR, Katz JS, Cavoto KK (1997) Pigeon perception and discrimination of rapidly changing texture stimuli. J Exp Psychol Anim Behav Process 23:390–400

    Article  CAS  PubMed  Google Scholar 

  • Cook RG, Katz JS, Blaisdell AP (2012) Temporal properties of visual search in pigeon target localization. J Exp Psychol Anim Behav Process 38:209–216

    Article  PubMed  Google Scholar 

  • Dalton P, Hughes RW (2014) Auditory attentional capture: implicit and explicit approaches. Psychol Res 78:313–320

    Article  PubMed  Google Scholar 

  • Davis ET, Palmer J (2004) Visual search and attention: an overview. Spat Vis 17:249–255

    Article  PubMed  Google Scholar 

  • de Bivort BL, van Swinderen B (2016) Evidence for selective attention in the insect brain. Curr Opin Insect Sci 15:9–15

    Article  PubMed  Google Scholar 

  • du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:131–146

    Article  PubMed  Google Scholar 

  • Dukas R, Kamil AC (2000) The cost of limited attention in blue jays. Behav Ecol 11:502–506

    Article  Google Scholar 

  • Duncan J, Humphreys GW (1989) Visual search and stimulus similarity. Psychol Rev 96:433–458

    Article  CAS  PubMed  Google Scholar 

  • Fitzke FW, Hayes BP, Hodos W, Holden AL, Low JC (1985) Refractive sectors in the visual field of the pigeon eye. J Physiol 369:33–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forster S, Lavie N (2016) Establishing the attention-distractibility trait. Psychol Sci 27:203–212

    Article  PubMed  Google Scholar 

  • Gutfreund Y (2012) Stimulus-specific adaptation, habituation and change detection in the gaze control system. Biol Cybern 106:657–668

    Article  PubMed  Google Scholar 

  • Harmening WM, Orlowski J, Ben-Shahar O, Wagner H (2011) Overt attention toward oriented objects in free-viewing barn owls. Proc Natl Acad Sci USA 108:8461–8466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hazan Y, Kra Y, Yarin I, Wagner H, Gutfreund Y (2015) Visual-auditory integration for visual search: a behavioral study in barn owls. Front Integr Neurosci 9:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Hickey C, McDonald JJ, Theeuwes J (2006) Electrophysiological evidence of the capture of visual attention. J Cogn Neurosci 18:604–613

    Article  PubMed  Google Scholar 

  • Hillyard SA, Stormer VS, Feng W, Martinez A, McDonald JJ (2016) Cross-modal orienting of visual attention. Neuropsychologia 83:170–178

    Article  PubMed  Google Scholar 

  • Ingle D (1975) Focal attention in the frog: behavioral and physiological correlates. Science 188:1033–1035

    Article  CAS  PubMed  Google Scholar 

  • Johnen A, Wagner H, Gaese BH (2001) Spatial attention modulates sound localization in barn owls. J Neurophysiol 85:1009–1012

    Article  CAS  PubMed  Google Scholar 

  • Knudsen EI (2011) Control from below: the role of a midbrain network in spatial attention. Eur J Neurosci 33:1961–1972

    Article  PubMed  PubMed Central  Google Scholar 

  • Knudsen EI, Blasdel GG, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol A 133:13–21

    Article  Google Scholar 

  • Koelewijn T, Bronkhorst A, Theeuwes J (2009) Auditory and visual capture during focused visual attention. J Exp Psychol Hum Percept Perform 35:1303–1315

    Article  PubMed  Google Scholar 

  • Krauzlis RJ, Liston D, Carello CD (2004) Target selection and the superior colliculus: goals, choices and hypotheses. Vis Res 44:1445–1451

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lavie N (1995) Perceptual load as a necessary condition for selective attention. J Exp Psychol Hum Percept Perform 21:451

    Article  CAS  PubMed  Google Scholar 

  • Lavie N (2005) Distracted and confused?: selective attention under load. Trends Cogn Sci 9:75–82

    Article  PubMed  Google Scholar 

  • Liesefeld HR, Liesefeld AM, Tollner T, Muller HJ (2017) Attentional capture in visual search: capture and post-capture dynamics revealed by EEG. Neuroimage 156:166–173

    Article  PubMed  Google Scholar 

  • Matusz PJ, Eimer M (2011) Multisensory enhancement of attentional capture in visual search. Psychon Bull Rev 18:904–909

    Article  PubMed  Google Scholar 

  • Matusz PJ, Broadbent H, Ferrari J, Forrest B, Merkley R, Scerif G (2015) Multi-modal distraction: insights from children’s limited attention. Cognition 136:156–165

    Article  PubMed  Google Scholar 

  • Mokeichev A, Segev R, Ben-Shahar O (2010) Orientation saliency without visual cortex and target selection in archer fish. Proc Natl Acad Sci USA 107:16726–16731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieder A, Wagner H (1999) Perception and neuronal coding of subjective contours in the owl. Nat Neurosci 2:660–663

    Article  CAS  PubMed  Google Scholar 

  • O’Carroll DC, Warrant EJ (2017) Vision in dim light: highlights and challenges. Philos Trans R Soc Lond B Biol Sci 372:1717

    Google Scholar 

  • Ohayon S, Harmening W, Wagner H, Rivlin E (2008) Through a barn owl’s eyes: interactions between scene content and visual attention. Biol Cybern 98:115–132

    Article  PubMed  Google Scholar 

  • Orlowski J, Beissel C, Rohn F, Adato Y, Wagner H, Ben-Shahar O (2015) Visual pop-out in barn owls: human-like behavior in the avian brain. J Vis 15:4

    Article  PubMed  Google Scholar 

  • Pinto Y, van der Leij AR, Sligte IG, Lamme VA, Scholte HS (2013) Bottom-up and top-down attention are independent. J Vis 13:16

    Article  PubMed  Google Scholar 

  • Sareen P, Wolf R, Heisenberg M (2011) Attracting the attention of a fly. Proc Natl Acad Sci USA 108:7230–7235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spaethe J, Tautz J, Chittka L (2006) Do honeybees detect colour targets using serial or parallel visual search? J Exp Biol 209:987–993

    Article  PubMed  Google Scholar 

  • Sridharan D, Ramamurthy DL, Schwarz JS, Knudsen EI (2014) Visuospatial selective attention in chickens. Proc Natl Acad Sci USA 111:E2056–E2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tellinghuisen DJ, Nowak EJ (2003) The inability to ignore auditory distractors as a function of visual task perceptual load. Percept Psychophys 65:817–828

    Article  PubMed  Google Scholar 

  • Theeuwes J (1992) Perceptual selectivity for color and form. Percept Psychophys 51:599–606

    Article  CAS  PubMed  Google Scholar 

  • Theeuwes J, Olivers CN, Belopolsky A (2010) Stimulus-driven capture and contingent capture. Wiley Interdiscip Rev Cogn Sci 1:872–881

    Article  PubMed  Google Scholar 

  • Treisman A, Gelade G (1980) A feature-integration theory of attention. Cogn Psychol 12:97–136

    Article  CAS  PubMed  Google Scholar 

  • Treisman A, Sato S (1990) Conjunction search revisited. J Exp Psychol Hum Percept Perform 16:459–478

    Article  CAS  PubMed  Google Scholar 

  • Wathey JC, Pettigrew JD (1989) Quantitative analysis of the retinal ganglion cell layer and optic nerve of the barn owl Tyto alba. Brain Behav Evol 33:279–292

    Article  CAS  PubMed  Google Scholar 

  • Wolfe JM, Horowitz TS (2004) What attributes guide the deployment of visual attention and how do they do it? Nat Rev Neurosci 5:495–501

    Article  CAS  PubMed  Google Scholar 

  • Wolfe JM, Cave KR, Franzel SL (1989) Guided search: an alternative to the feature integration model for visual search. J Exp Psychol Hum Percept Perform 15:419–433

    Article  CAS  PubMed  Google Scholar 

  • Zentall TR (2005) Selective and divided attention in animals. Behav Processes 69:1–15

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Yael Zahar for technical and graphical support. We would also like to thank Prof. Herman Wagner and Julius Orlowski from Aachen University for their support in constructing the headcam for barn owls.

Funding

This study was funded by Grants to Yoram Gutfreund from the Israel Science Foundation, the Adelis Foundation and the Rappaport Institute research grant.

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Correspondence to Yoram Gutfreund.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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This article does not contain any studies with human participants performed by any of the authors.

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Lev-Ari, T., Gutfreund, Y. Interactions between top-down and bottom-up attention in barn owls (Tyto alba). Anim Cogn 21, 197–205 (2018). https://doi.org/10.1007/s10071-017-1150-2

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  • DOI: https://doi.org/10.1007/s10071-017-1150-2

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