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Home / Equine Research Bank / Sci Rep / Spontaneous eye blinks in horses (Equus caballus) are modula...
Scientific reports2024; 14(1); 19336; doi: 10.1038/s41598-024-70141-y

Spontaneous eye blinks in horses (Equus caballus) are modulated by attention.

Abstract: Spontaneous eye blinks are brief closures of both eyelids. The spontaneous eye blink rate (SEBR) exceeds physiological corneal needs and is modulated by emotions and cognitive states, including vigilance and attention, in humans. In several animal species, the SEBR is modulated by stress and antipredator vigilance, which may limit the loss of visual information due to spontaneous eye closing. Here, we investigated whether the SEBR is modulated by attention in the domestic horse (Equus caballus). Our data supported previous studies indicating a tonic SEBR specific to each individual. We also found that, superimposed on a tonic SEBR, phasic changes were induced by cognitive processing. Attention downmodulated the SEBR, with the magnitude of blink inhibition proportional to the degree of attentional selectivity. On the other hand, reward anticipation upregulated the SEBR. Our data also suggested that horses possess the cognitive property of object permanence: they understand that an object that is no longer in their visual field has not ceased to exist. In conclusion, our results suggested that spontaneous eye blinks in horses are modulated by attentional cognitive processing.
© 2024. The Author(s).
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Publication Date: 2024-08-20 PubMed ID: 39164361PubMed Central: PMC11336180DOI: 10.1038/s41598-024-70141-yGoogle Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research paper explores how the rate of spontaneous eye blinks in horses may be influenced by the animal’s attention. The study found that both attention and the anticipation of rewards modulate a horse’s eye blink rate, suggesting blinks are tied to cognitive processing in this species.

Research Context

  • The study focuses on spontaneous eye blink rate (SEBR), which are short moments when both eyelids close involuntarily. This rate exceeds the necessary blinks for physiological needs such as corneal moisture.
  • In humans, changes in the SEBR are known to be tied to emotional and cognitive factors, including vigilance and attention.
  • Other animal species also exhibit changes in SEBR due to stress or antipredator behavior as a way to limit loss of visual information. This research examines whether a similar modulation happens in horses based on their attention.

Research Findings

  • The research supports earlier studies that suggested each individual horse has its own distinct, steady (tonic) SEBR.
  • Beyond this tonic rate, the horse’s SEBR also exhibits temporary (phasic) changes based on cognitive processing.
  • When a horse focuses its attention, the SEBR decreases, with the level of reduction connected to how selective the attention is.
  • Anticipation of a reward, on the other hand, was found to cause an increase in the SEBR.
  • Further, the study suggests that horses possess object permanence: they understand that an object is not gone just because it is no longer in their sight. This is another example of cognition influencing SEBR.

Conclusions

  • This study concludes that horses’ blink rate is influenced by cognitive processing in terms of their attention.
  • This reinforces the existing understanding that SEBR is not just about physical needs like cornea moisture, but is also connected to mental processes, at least in certain species.
  • Given the relationship of blink rate to attention, variations in a horse’s SEBR may provide some insight into the animal’s cognitive state.

Cite This Article

APA
Tomberg C, Petagna M, de Selliers de Moranville LA. (2024). Spontaneous eye blinks in horses (Equus caballus) are modulated by attention. Sci Rep, 14(1), 19336. https://doi.org/10.1038/s41598-024-70141-y

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 14
Issue: 1
Pages: 19336
PII: 19336

Researcher Affiliations

Tomberg, Claude
  • Faculty of Medicine, Université libre de Bruxelles, 808, route de Lennik, CP 630, 1070, Brussels, Belgium. claude.tomberg@ulb.be.
Petagna, Maxime
  • Faculty of Medicine, Université libre de Bruxelles, 808, route de Lennik, CP 630, 1070, Brussels, Belgium.
de Selliers de Moranville, Lucy-Anne
  • Faculty of Medicine, Université libre de Bruxelles, 808, route de Lennik, CP 630, 1070, Brussels, Belgium.

MeSH Terms

  • Animals
  • Horses / physiology
  • Blinking / physiology
  • Attention / physiology
  • Male
  • Female
  • Cognition / physiology

Grant Funding

  • Convention 1-5 / Fondation Prince Laurent

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 131 references
  1. Cruz AA, Garcia DM, Pinto CT, Cechetti SP. Spontaneous eyeblink activity. Ocul. Surf. 9, 29–41 (2011).
    doi: 10.1016/S1542-0124(11)70007-6pubmed: 21338567google scholar: lookup
  2. Moss HE. Eyelid and facial nerve disorders. In Liu, Volpe, and Galetta’s Neuro-Ophthalmology (ed. Moss, H. E.) (Elsevier, 2019).
  3. Ponder E, Kennedy WP. On the act of blinking. Q. J. Exp. Physiol. 18, 89–110 (1927).
    doi: 10.1113/expphysiol.1927.sp000433google scholar: lookup
  4. Zametkin AJ, Stevens JR, Pittman R. Ontogeny of spontaneous blinking and of habituation of the blink reflex. Ann. Neurol. 5, 453–457 (1979).
    doi: 10.1002/ana.410050509pubmed: 223495google scholar: lookup
  5. Oh J, Jeong SY, Jeong J. The timing and temporal patterns of eye blinking are dynamically modulated by attention. Hum. Mov. Sci. 31, 1353–1365 (2012).
    doi: 10.1016/j.humov.2012.06.003pubmed: 22877514google scholar: lookup
  6. Rodriguez JD. Blink: Characteristics, controls, and relation to dry eyes. Curr. Eye Res. 43, 52–66 (2018).
    doi: 10.1080/02713683.2017.1381270pubmed: 29043838google scholar: lookup
  7. Bentivoglio AR. Analysis of blink rate patterns in normal subjects. Mov. Disord. 12, 1028–1034 (1997).
    doi: 10.1002/mds.870120629pubmed: 9399231google scholar: lookup
  8. Van Slooten JC, Jahfari S, Theeuwes J. Spontaneous eye blink rate predicts individual differences in exploration and exploitation during reinforcement learning. Sci. Rep. 9, 17436 (2019).
    doi: 10.1038/s41598-019-53805-ypmc: PMC6874684pubmed: 31758031google scholar: lookup
  9. Gergelyfi M, Jacob B, Olivier E, Zénon A. Dissociation between mental fatigue and motivational state during prolonged mental activity. Front. Behav. Neurosci. 10.3389/fnbeh.2015.00176 (2015).
    doi: 10.3389/fnbeh.2015.00176pmc: PMC4499755pubmed: 26217203google scholar: lookup
  10. Horiuchi R, Ogasawara T, Miki N. Fatigue assessment by blink detected with attachable optical sensors of dye-sensitized photovoltaic cells. Micromachines 9, 310 (2018).
    doi: 10.3390/mi9060310pmc: PMC6187843pubmed: 30424243google scholar: lookup
  11. ZargariMarandi R, Madeleine P, Omland Ø, Vuillerme N, Samani A. An oculometrics-based biofeedback system to impede fatigue development during computer work: A proof-of-concept study. PLoS ONE 14, e0213704 (2019).
    doi: 10.1371/journal.pone.0213704pmc: PMC6544207pubmed: 31150405google scholar: lookup
  12. Giannakakis G. Stress and anxiety detection using facial cues from videos. Biomed. Signal Process. Control 31, 89–101 (2017).
    doi: 10.1016/j.bspc.2016.06.020google scholar: lookup
  13. Maffei A, Angrilli A. Spontaneous eye blink rate: An index of dopaminergic component of sustained attention and fatigue. Int. J. Psychophysiol. 123, 58–63 (2018).
    doi: 10.1016/j.ijpsycho.2017.11.009pubmed: 29133149google scholar: lookup
  14. Magliacano A, Fiorenza S, Estraneo A, Trojano L. Eye blink rate increases as a function of cognitive load during an auditory oddball paradigm. Neurosci. Lett. 736, 135293 (2020).
    doi: 10.1016/j.neulet.2020.135293pubmed: 32771601google scholar: lookup
  15. McMonnies CW. Blinking mechanisms. In Encyclopedia of the Eye (ed. McMonnies, C. W.) (Elsevier, 2010).
  16. Kahneman D. Attention and Effort. (Prentice-Hall, 1973).
  17. Baumstimler Y, Parrot J. Stimulus generalization and spontaneous blinking in man involved in a voluntary activity. J. Exp. Psychol. 88, 95–102 (1971).
    doi: 10.1037/h0030638google scholar: lookup
  18. Nakano T, Kato M, Morito Y, Itoi S, Kitazawa S. Blink-related momentary activation of the default mode network while viewing videos. Proc. Natl. Acad. Sci. 110, 702–706 (2013).
    doi: 10.1073/pnas.1214804110pmc: PMC3545766pubmed: 23267078google scholar: lookup
  19. Stern JA, Walrath LC, Goldstein R. The endogenous eyeblink. Psychophysiology 21, 22–33 (1984).
    doi: 10.1111/j.1469-8986.1984.tb02312.xpubmed: 6701241google scholar: lookup
  20. Nakano T, Kitazawa S. Eyeblink entrainment at breakpoints of speech. Exp. Brain Res. 205, 577–581 (2010).
    doi: 10.1007/s00221-010-2387-zpubmed: 20700731google scholar: lookup
  21. Fogarty C, Stern JA. Eye movements and blinks: Their relationship to higher cognitive processes. Int. J. Psychophysiol. 8, 35–42 (1989).
    doi: 10.1016/0167-8760(89)90017-2pubmed: 2584081google scholar: lookup
  22. Riggs LA, Volkmann FC, Moore RK. Suppression of the blackout due to blinks. Vis. Res. 21, 1075–1079 (1981).
    doi: 10.1016/0042-6989(81)90012-2pubmed: 7314488google scholar: lookup
  23. Tada H, Omori Y, Hirokawa K, Ohira H, Tomonaga M. Eye-blink behaviors in 71 species of primates. PLoS ONE 8, e66018 (2013).
    doi: 10.1371/journal.pone.0066018pmc: PMC3669291pubmed: 23741522google scholar: lookup
  24. Matsumoto-Oda A, Okamoto K, Takahashi K, Ohira H. Group size effects on inter-blink interval as an indicator of antipredator vigilance in wild baboons. Sci. Rep. 8, 10062 (2018).
    doi: 10.1038/s41598-018-28174-7pmc: PMC6030190pubmed: 29968733google scholar: lookup
  25. Rowe ZW, Robins JH, Rands SA. Red deer Cervuselaphus blink more in larger groups. Ecol. Evol. 13, e9908 (2023).
    doi: 10.1002/ece3.9908pmc: PMC10015368pubmed: 36937074google scholar: lookup
  26. Beauchamp G. Half-blind to the risk of predation. Front. Ecol. Evol. 5, 131 (2017).
    doi: 10.3389/fevo.2017.00131google scholar: lookup
  27. Yorzinski JL. Eye blinking in an avian species is associated with gaze shifts. Sci. Rep. 6, 32471 (2016).
    doi: 10.1038/srep32471pmc: PMC5004160pubmed: 27572457google scholar: lookup
  28. Cross DJ. Distinct neural circuits underlie assessment of a diversity of natural dangers by American crows. Proc. R. Soc. B Biol. Sci. 280, 20131046 (2013).
    doi: 10.1098/rspb.2013.1046pmc: PMC3712449pubmed: 23825209google scholar: lookup
  29. Yorzinski JL, Walker MK, Cavalier RA. A songbird strategically modifies its blinking behavior when viewing human faces. Anim. Cogn. 24, 787–801 (2021).
    doi: 10.1007/s10071-021-01476-6pubmed: 33501597google scholar: lookup
  30. Lim J, Dinges DF. Sleep deprivation and vigilant attention. Ann. N. Y. Acad. Sci. 1129, 305–322 (2008).
    doi: 10.1196/annals.1417.002pubmed: 18591490google scholar: lookup
  31. Robertson IH, Garavan H. Vigilant attention. In The Cognitive Neurosciences (eds Robertson, I. H. & Garavan, H.) (Boston Review, 2004).
  32. Dimond S, Lazarus J. The problem of vigilance in animal life. Brain Behav. Evol. 9, 60–79 (1974).
    doi: 10.1159/000123655pubmed: 4847593google scholar: lookup
  33. Van Schie MKM, Lammers GJ, Fronczek R, Middelkoop HAM, Van Dijk JG. Vigilance: Discussion of related concepts and proposal for a definition. Sleep Med. 83, 175–181 (2021).
    doi: 10.1016/j.sleep.2021.04.038pubmed: 34022494google scholar: lookup
  34. Beauchamp G. Overview of animal vigilance. In Animal Vigilance (ed. Beauchamp, G.) (Elsevier, 2015).
  35. Klösch G, Zeitlhofer J, Ipsiroglu O. Revisiting the concept of vigilance. Front. Psychiatr. 13, 874757 (2022).
    doi: 10.3389/fpsyt.2022.874757pmc: PMC9237243pubmed: 35774096google scholar: lookup
  36. Head H. The conception of nervous and mental energy. (II.) ‘Vigilance; a physiological state of the nervous system’. Br. J. Psychol. 14, 126–147 (1923).
  37. Canisius S, Penzel T. Vigilance monitoring—Review and practical aspects. Biomed. Tech. Eng. 52, 77–82 (2007).
    doi: 10.1515/BMT.2007.015pubmed: 17313339google scholar: lookup
  38. Bremer F. Cerebral hypnogenic centers. Ann. Neurol. 2, 1–6 (1977).
    doi: 10.1002/ana.410020102pubmed: 900903google scholar: lookup
  39. Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455–473 (1949).
    doi: 10.1016/0013-4694(49)90219-9pubmed: 18421835google scholar: lookup
  40. Darby CV, Guilleminault C. Encyclopedia of Sleep and Circadian Rhythms. ScienceDirect http://www.sciencedirect.com:5070/referencework/9780323910941/encyclopedia-of-sleep-and-circadian-rhythms.
  41. Jasper H. Diffuse projection systems: The integrative action of the thalamic reticular system. Electroencephalogr. Clin. Neurophysiol. 1, 405–420 (1949).
    doi: 10.1016/0013-4694(49)90213-8pubmed: 18421831google scholar: lookup
  42. Llinás RR, Steriade M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297–3308 (2006).
    doi: 10.1152/jn.00166.2006pubmed: 16554502google scholar: lookup
  43. Steriade M. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101, 243–276 (2000).
    doi: 10.1016/S0306-4522(00)00353-5pubmed: 11074149google scholar: lookup
  44. Magliacano A. Spontaneous eye blinking as a diagnostic marker in prolonged disorders of consciousness. Sci. Rep. 11, 22393 (2021).
    doi: 10.1038/s41598-021-01858-3pmc: PMC8599689pubmed: 34789832google scholar: lookup
  45. Panda R. Disruption in structural–functional network repertoire and time-resolved subcortical fronto-temporoparietal connectivity in disorders of consciousness. eLife 11, e77462 (2022).
    doi: 10.7554/eLife.77462pmc: PMC9385205pubmed: 35916363google scholar: lookup
  46. Oken BS, Salinsky MC, Elsas SM. Vigilance, alertness, or sustained attention: Physiological basis and measurement. Clin. Neurophysiol. 117, 1885–1901 (2006).
    doi: 10.1016/j.clinph.2006.01.017pmc: PMC2865224pubmed: 16581292google scholar: lookup
  47. Posner MI, Petersen SE. The attention system of the human brain. Annu. Rev. Neurosci. 13, 25–42 (1990).
    doi: 10.1146/annurev.ne.13.030190.000325pubmed: 2183676google scholar: lookup
  48. Clarke DD, Sokoloff L. Circulation and energy metabolism of the brain. In Basic Neurochemistry: Molecular, Cellular and Medical Aspects (eds Clarke, D. D. & Sokoloff, L.) (Lippincott-Raven, 1999).
  49. Carrasco M. Visual attention: The past 25 years. Vis. Res. 51, 1484–1525 (2011).
    doi: 10.1016/j.visres.2011.04.012pmc: PMC3390154pubmed: 21549742google scholar: lookup
  50. Raymond JE, Shapiro KL, Arnell KM. Temporary suppression of visual processing in an RSVP task: An attentional blink?. J. Exp. Psychol. Hum. Percept. Perform. 18, 849–860 (1992).
    doi: 10.1037/0096-1523.18.3.849pubmed: 1500880google scholar: lookup
  51. Hillyard SA, Vogel EK, Luck SJ. Sensory gain control (amplification) as a mechanism of selective attention: Electrophysiological and neuroimaging evidence. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353, 1257–1270 (1998).
    doi: 10.1098/rstb.1998.0281pmc: PMC1692341pubmed: 9770220google scholar: lookup
  52. Tomberg C, Desmedt JE. Non-averaged human brain potentials in somatic attention: The short-latency cognition-related P40 component. J. Physiol. 496, 559–574 (1996).
    doi: 10.1113/jphysiol.1996.sp021707pmc: PMC1160899pubmed: 8910238google scholar: lookup
  53. Lennie P. The cost of cortical computation. Curr. Biol. 13, 493–497 (2003).
    doi: 10.1016/S0960-9822(03)00135-0pubmed: 12646132google scholar: lookup
  54. Desmedt JE, Tomberg C. Mapping early somatosensory evoked potentials in selective attention: Critical evaluation of control conditions used for titrating by difference the cognitive P30, P40, P100 and N140. Electroencephalogr. Clin. Neurophysiol. Potentials Sect. 74, 321–346 (1989).
    doi: 10.1016/0168-5597(89)90001-4pubmed: 2476292google scholar: lookup
  55. Mangun GR, Hillyard SA. Allocation of visual attention to spatial locations: Tradeoff functions for event-related brain potentials and detection performance. Percept. Psychophys. 47, 532–550 (1990).
    doi: 10.3758/BF03203106pubmed: 2367174google scholar: lookup
  56. Mountcastle VB. Brain mechanisms for directed attention. J. R. Soc. Med. 71, 14–28 (1978).
    doi: 10.1177/014107687807100105pmc: PMC1436420pubmed: 416210google scholar: lookup
  57. Müller NG, Bartelt OA, Donner TH, Villringer A, Brandt SA. A physiological correlate of the “zoom lens” of visual attention. J. Neurosci. 23, 3561–3565 (2003).
    doi: 10.1523/JNEUROSCI.23-09-03561.2003pmc: PMC6742201pubmed: 12736325google scholar: lookup
  58. Maunsell JHR. Neuronal mechanisms of visual attention. Annu. Rev. Vis. Sci. 1, 373–391 (2015).
    doi: 10.1146/annurev-vision-082114-035431pmc: PMC8279254pubmed: 28532368google scholar: lookup
  59. Beecher MD, Harrison JM. Rapid acquisition of an auditory localization discrimination by rats 1. J. Exp. Anal. Behav. 16, 193–199 (1971).
    doi: 10.1901/jeab.1971.16-193pmc: PMC1333867pubmed: 5121856google scholar: lookup
  60. Roberts SM. Equine vision and optics. Vet. Clin. North Am. Equine Pract. 8, 451–457 (1992).
    doi: 10.1016/S0749-0739(17)30435-2pubmed: 1458323google scholar: lookup
  61. Lundblad J, Rashid M, Rhodin M, Haubro Andersen P. Effect of transportation and social isolation on facial expressions of healthy horses. PLoS ONE 16, e0241532 (2021).
    doi: 10.1371/journal.pone.0241532pmc: PMC8177539pubmed: 34086704google scholar: lookup
  62. Merkies K, Ready C, Farkas L, Hodder A. Eye blink rates and eyelid twitches as a non-invasive measure of stress in the domestic horse. Animals 9, 562 (2019).
    doi: 10.3390/ani9080562pmc: PMC6721043pubmed: 31443315google scholar: lookup
  63. Mott RO, Hawthorne SJ, McBride SD. Blink rate as a measure of stress and attention in the domestic horse (Equuscaballus). Sci. Rep. 10, 21409 (2020).
    doi: 10.1038/s41598-020-78386-zpmc: PMC7722727pubmed: 33293559google scholar: lookup
  64. Roberts K, Hemmings AJ, Moore-Colyer M, Parker MO, McBride SD. Neural modulators of temperament: A multivariate approach to personality trait identification in the horse. Physiol. Behav. 167, 125–131 (2016).
    doi: 10.1016/j.physbeh.2016.08.029pubmed: 27597134google scholar: lookup
  65. Cherry RL, Adair HS, Chen T, Hendrix DV, Ward DA. Effect of attentional focus levels on spontaneous eyeblink rate in horses. Vet. Ophthalmol. 23, 690–695 (2020).
    doi: 10.1111/vop.12778pubmed: 32437053google scholar: lookup
  66. Baragli P, Scopa C, Maglieri V, Palagi E. If horses had toes: Demonstrating mirror self recognition at group level in Equuscaballus. Anim. Cogn. 24, 1099–1108 (2021).
    doi: 10.1007/s10071-021-01502-7pmc: PMC8360890pubmed: 33713273google scholar: lookup
  67. Wathan J, McComb K. The eyes and ears are visual indicators of attention in domestic horses. Curr. Biol. 24, R677–R679 (2014).
    doi: 10.1016/j.cub.2014.06.023pmc: PMC4123162pubmed: 25093554google scholar: lookup
  68. Tomberg C, Petagna M, De Selliers De Moranville LA. Horses (Equuscaballus) facial micro-expressions: Insight into discreet social information. Sci. Rep. 13, 8625 (2023).
    doi: 10.1038/s41598-023-35807-zpmc: PMC10224940pubmed: 37244937google scholar: lookup
  69. Rochais C. A novel test for evaluating horses’ spontaneous visual attention is predictive of attention in operant learning tasks. Sci. Nat. 104, 61 (2017).
    doi: 10.1007/s00114-017-1480-6pubmed: 28681089google scholar: lookup
  70. Rochais C, Henry S, Hausberger M. Spontaneous attention-capture by auditory distractors as predictor of distractibility: A study of domestic horses (Equuscaballus). Sci. Rep. 7, 15283 (2017).
    doi: 10.1038/s41598-017-15654-5pmc: PMC5681571pubmed: 29127367google scholar: lookup
  71. Doughty MJ. Further assessment of gender- and blink pattern-related differences in the spontaneous eyeblink activity in primary gaze in young adult humans. Optom. Vis. Sci. 79, 439–447 (2002).
    doi: 10.1097/00006324-200207000-00013pubmed: 12137399google scholar: lookup
  72. Corujo LA, Kieson E, Schloesser T, Gloor PA. Emotion recognition in horses with convolutional neural networks. Future Internet 13, 250 (2021).
    doi: 10.3390/fi13100250google scholar: lookup
  73. Carrington SD, Bedford PGC, Guillon JP, Woodward EG. Polarized light biomicroscopic observations on the pre-corneal tear film. 1. The normal tear film of the dog. J. Small Anim. Pract. 28, 605–622 (1987).
    doi: 10.1111/j.1748-5827.1987.tb01276.xgoogle scholar: lookup
  74. Jongkees BJ, Colzato LS. Spontaneous eye blink rate as predictor of dopamine-related cognitive function—A review. Neurosci. Biobehav. Rev. 71, 58–82 (2016).
    doi: 10.1016/j.neubiorev.2016.08.020pubmed: 27555290google scholar: lookup
  75. Momozawa Y, Takeuchi Y, Kusunose R, Kikusui T, Mori Y. Association between equine temperament and polymorphisms in dopamine D4 receptor gene. Mamm. Genome 16, 538–544 (2005).
    doi: 10.1007/s00335-005-0021-3pubmed: 16151699google scholar: lookup
  76. Bacher LF, Allen KJ. Sensitivity of the rate of spontaneous eye blinking to type of stimuli in young infants. Dev. Psychobiol. 51, 186–197 (2009).
    doi: 10.1002/dev.20357pubmed: 19062172google scholar: lookup
  77. Unsworth N, Robison MK, Miller AL. Individual differences in baseline oculometrics: Examining variation in baseline pupil diameter, spontaneous eye blink rate, and fixation stability. Cogn. Affect. Behav. Neurosci. 10.3758/s13415-019-00709-z (2019).
    doi: 10.3758/s13415-019-00709-zpubmed: 30888645google scholar: lookup
  78. Dreisbach G. Dopamine and cognitive control: The influence of spontaneous eyeblink rate and dopamine gene polymorphisms on perseveration and distractibility. Behav. Neurosci. 119, 483–490 (2005).
    doi: 10.1037/0735-7044.119.2.483pubmed: 15839794google scholar: lookup
  79. Müller J. Dopamine and cognitive control: The influence of spontaneous eyeblink rate, DRD4 exon III polymorphism and gender on flexibility in set-shifting. Brain Res. 1131, 155–162 (2007).
    doi: 10.1016/j.brainres.2006.11.002pubmed: 17156756google scholar: lookup
  80. Colzato LS, van den Wildenberg WPM, van Wouwe NC, Pannebakker MM, Hommel B. Dopamine and inhibitory action control: Evidence from spontaneous eye blink rates. Exp. Brain Res. 196, 467–474 (2009).
    doi: 10.1007/s00221-009-1862-xpmc: PMC2700244pubmed: 19484465google scholar: lookup
  81. Lansade L, Simon F. Horses’ learning performances are under the influence of several temperamental dimensions. Appl. Anim. Behav. Sci. 125, 30–37 (2010).
    doi: 10.1016/j.applanim.2010.02.010google scholar: lookup
  82. de JesúsTello-Pasos A, González-Pech PG, Leste-Lasserre C, Pacheco AO. An exploratory study of negative and positive facial expressions of carriage horses during their nocturnal resting. J. Vet. Behav. 10.1016/j.jveb.2022.11.006 (2022).
    doi: 10.1016/j.jveb.2022.11.006google scholar: lookup
  83. Lansade L. Facial expression and oxytocin as possible markers of positive emotions in horses. Sci. Rep. 8, 14680 (2018).
    doi: 10.1038/s41598-018-32993-zpmc: PMC6168541pubmed: 30279565google scholar: lookup
  84. Hall A. The origin and purposes of blinking. Br. J. Ophthalmol. 29, 445–467 (1945).
    doi: 10.1136/bjo.29.9.445pmc: PMC510520pubmed: 18170143google scholar: lookup
  85. Orchard LN, Stern JA. Blinks as an index of cognitive activity during reading. Integr. Physiol. Behav. Sci. 26, 108–116 (1991).
    doi: 10.1007/BF02691032pubmed: 1878317google scholar: lookup
  86. Nakano T, Yamamoto Y, Kitajo K, Takahashi T, Kitazawa S. Synchronization of spontaneous eyeblinks while viewing video stories. Proc. R. Soc. B Biol. Sci. 276, 3635–3644 (2009).
    doi: 10.1098/rspb.2009.0828pmc: PMC2817301pubmed: 19640888google scholar: lookup
  87. Van Opstal F, De Loof E, Verguts T, Cleeremans A. Spontaneous eyeblinks during breaking continuous flash suppression are associated with increased detection times. J. Vis. 16, 21 (2016).
    doi: 10.1167/16.14.21pubmed: 27902828google scholar: lookup
  88. Goossens HHLM, Van Opstal AJ. Blink-perturbed saccades in monkey I. Behavioral analysis. J. Neurophysiol. 83, 3411–3429 (2000).
    doi: 10.1152/jn.2000.83.6.3411pubmed: 10848559google scholar: lookup
  89. Wallace DJ. Rats maintain an overhead binocular field at the expense of constant fusion. Nature 498, 65–69 (2013).
    doi: 10.1038/nature12153pubmed: 23708965google scholar: lookup
  90. Evans KE, McGreevy PD. The distribution of ganglion cells in the equine retina and its relationship to skull morphology. Anat. Histol. Embryol. 36, 151–156 (2007).
    doi: 10.1111/j.1439-0264.2006.00749.xpubmed: 17371390google scholar: lookup
  91. Guo X, Sugita S. Topography of ganglion cells in the retina of the horse. J. Vet. Med. Sci. 62, 1145–1150 (2000).
    doi: 10.1292/jvms.62.1145pubmed: 11129856google scholar: lookup
  92. Harman AM, Moore S, Hoskins R, Keller P. Horse vision and an explanation for the visual behaviour originally explained by the ‘ramp retina’. Equine Vet. J. 31, 384–390 (1999).
    doi: 10.1111/j.2042-3306.1999.tb03837.xpubmed: 10505953google scholar: lookup
  93. Hebel R. Distribution of retinal ganglion cells in five mammalian species (pig, sheep, ox, horse, dog). Anat. Embryol. (Berl.) 150, 45–51 (1976).
    doi: 10.1007/BF00346285pubmed: 1015629google scholar: lookup
  94. Baillargeon R. Innate ideas revisited: For a principle of persistence in infants’ physical reasoning. Perspect. Psychol. Sci. 3, 2–13 (2008).
    doi: 10.1111/j.1745-6916.2008.00056.xpmc: PMC3357323pubmed: 22623946google scholar: lookup
  95. Piaget J. The Construction of Reality in the Child. (Basic Books, 1954).
  96. Bremner JG, Slater AM, Johnson SP. Perception of object persistence: The origins of object permanence in infancy. Child Dev. Perspect. 9, 7–13 (2015).
    doi: 10.1111/cdep.12098google scholar: lookup
  97. Bremhorst A, Sutter NA, Würbel H, Mills DS, Riemer S. Differences in facial expressions during positive anticipation and frustration in dogs awaiting a reward. Sci. Rep. 9, 19312 (2019).
    doi: 10.1038/s41598-019-55714-6pmc: PMC6917793pubmed: 31848389google scholar: lookup
  98. McPeake KJ, Collins LM, Zulch H, Mills DS. The canine frustration questionnaire—Development of a new psychometric tool for measuring frustration in domestic dogs (Canisfamiliaris). Front. Vet. Sci. 6, 152 (2019).
    doi: 10.3389/fvets.2019.00152pmc: PMC6535675pubmed: 31165075google scholar: lookup
  99. Scopa C, Maglieri V, Baragli P, Palagi E. Getting rid of blinkers: The case of mirror self-recognition in horses (Equuscaballus). Anim. Cogn. 25, 711–716 (2022).
    doi: 10.1007/s10071-022-01638-0pubmed: 35704243google scholar: lookup
  100. Ringhofer M, Yamamoto S. Domestic horses send signals to humans when they face with an unsolvable task. Anim. Cogn. 20, 397–405 (2017).
    doi: 10.1007/s10071-016-1056-4pubmed: 27885519google scholar: lookup
  101. Trösch. Horses categorize human emotions cross-modally based on facial expression and non-verbal vocalizations. Animals 9, 862 (2019).
    doi: 10.3390/ani9110862pmc: PMC6912773pubmed: 31653088google scholar: lookup
  102. Rochais C. Visual attention, an indicator of human-animal relationships? A study of domestic horses (Equuscaballus). Front. Psychol. 10.3389/fpsyg.2014.00108 (2014).
    doi: 10.3389/fpsyg.2014.00108pmc: PMC3923161pubmed: 24592244google scholar: lookup
  103. Gavas R. Blink rate variability: a marker of sustained attention during a visual task. in Adjunct Proceedings of the 2020 ACM International Joint Conference on Pervasive and Ubiquitous Computing and Proceedings of the 2020 ACM International Symposium on Wearable Computers 450–455 (ACM, Virtual Event Mexico, 2020).
    doi: 10.1145/3410530.3414431google scholar: lookup
  104. Pivik RT, Dykman RA. Endogenous eye blinks in preadolescents: Relationship to information processing and performance. Biol. Psychol. 66, 191–219 (2004).
    doi: 10.1016/j.biopsycho.2003.10.005pubmed: 15099694google scholar: lookup
  105. Ballesta S, Mosher CP, Szep J, Fischl KD, Gothard KM. Social determinants of eyeblinks in adult male macaques. Sci. Rep. 6, 38686 (2016).
    doi: 10.1038/srep38686pmc: PMC5138631pubmed: 27922101google scholar: lookup
  106. Shultz S, Klin A, Jones W. Inhibition of eye blinking reveals subjective perceptions of stimulus salience. Proc. Natl. Acad. Sci. 108, 21270–21275 (2011).
    doi: 10.1073/pnas.1109304108pmc: PMC3248475pubmed: 22160686google scholar: lookup
  107. Blount WP. Studies of the movements of the eyelids of animals: Blinking. Q. J. Exp. Physiol. 18, 111–125 (1927).
    doi: 10.1113/expphysiol.1927.sp000426google scholar: lookup
  108. Karson CN. Spontaneous eye-blink rates and dopaminergic systems. Brain 106, 643–653 (1983).
    doi: 10.1093/brain/106.3.643pubmed: 6640274google scholar: lookup
  109. Lawrence MS, Redmond DE. MPTP lesions and dopaminergic drugs alter eye blink rate in African green monkeys. Pharmacol. Biochem. Behav. 38, 869–874 (1991).
    doi: 10.1016/0091-3057(91)90255-Zpubmed: 1678527google scholar: lookup
  110. Elsworth JD. D1 and D2 dopamine receptors independently regulate spontaneous blink rate in the vervet monkey. J. Pharmacol. Exp. Ther. 259, 595–600 (1991).
    pubmed: 1682479
  111. Kaminer J, Powers AS, Horn KG, Hui C, Evinger C. Characterizing the spontaneous blink generator: An animal model. J. Neurosci. 31, 11256–11267 (2011).
    doi: 10.1523/JNEUROSCI.6218-10.2011pmc: PMC3156585pubmed: 21813686google scholar: lookup
  112. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).
    doi: 10.1126/science.275.5306.1593pubmed: 9054347google scholar: lookup
  113. Thiele A, Bellgrove MA. Neuromodulation of attention. Neuron 97, 769–785 (2018).
    doi: 10.1016/j.neuron.2018.01.008pmc: PMC6204752pubmed: 29470969google scholar: lookup
  114. Peckham AD, Johnson SL. Spontaneous eye-blink rate as an index of reward responsivity: Validation and links to bipolar disorder. Clin. Psychol. Sci. 4, 451–463 (2016).
    doi: 10.1177/2167702615594999pmc: PMC4886748pubmed: 27274949google scholar: lookup
  115. Anderson BA. The role of dopamine in value-based attentional orienting. Curr. Biol. 26, 550–555 (2016).
    doi: 10.1016/j.cub.2015.12.062pmc: PMC4767677pubmed: 26877079google scholar: lookup
  116. Yamaguchi Y. Dopamine-dependent visual attention preference to social stimuli in nonhuman primates. Psychopharmacol. (Berl.) 234, 1113–1120 (2017).
    doi: 10.1007/s00213-017-4544-6pmc: PMC5352745pubmed: 28154891google scholar: lookup
  117. Kroener S, Chandler LJ, Phillips PE, Seamans JK. Dopamine modulates persistent synaptic activity and enhances the signal-to-noise ratio in the prefrontal cortex. PLoS ONE 4, e6507 (2009).
    doi: 10.1371/journal.pone.0006507pmc: PMC2715878pubmed: 19654866google scholar: lookup
  118. Vander Weele CM. Dopamine enhances signal-to-noise ratio in cortical-brainstem encoding of aversive stimuli. Nature 563, 397–401 (2018).
    doi: 10.1038/s41586-018-0682-1pmc: PMC6645392pubmed: 30405240google scholar: lookup
  119. Lockhofen DEL, Mulert C. Neurochemistry of visual attention. Front. Neurosci. 15, 643597 (2021).
    doi: 10.3389/fnins.2021.643597pmc: PMC8133366pubmed: 34025339google scholar: lookup
  120. Lesimple C, Sankey C, Richard MA, Hausberger M. Do horses expect humans to solve their problems?. Front. Psychol. 3, 306 (2012).
    doi: 10.3389/fpsyg.2012.00306pmc: PMC3426792pubmed: 22936923google scholar: lookup
  121. Niv Y, Daw ND, Joel D, Dayan P. Tonic dopamine: Opportunity costs and the control of response vigor. Psychopharmacol. (Berl.) 191, 507–520 (2007).
    doi: 10.1007/s00213-006-0502-4pubmed: 17031711google scholar: lookup
  122. Pas P, Custers R, Bijleveld E, Vink M. Effort responses to suboptimal reward cues are related to striatal dopaminergic functioning. Motiv. Emot. 38, 759–770 (2014).
    doi: 10.1007/s11031-014-9434-1pmc: PMC4223541pubmed: 25400304google scholar: lookup
  123. Den Daas C, Häfner M, De Wit J. Out of sight, out of mind: Cognitive states alter the focus of attention. Exp. Psychol. 60, 313–323 (2013).
    doi: 10.1027/1618-3169/a000201pubmed: 23628695google scholar: lookup
  124. McBride SD, Roberts K, Hemmings AJ, Ninomiya S, Parker MO. The impulsive horse: Comparing genetic, physiological and behavioral indicators to those of human addiction. Physiol. Behav. 254, 113896 (2022).
    doi: 10.1016/j.physbeh.2022.113896pubmed: 35777460google scholar: lookup
  125. Stratton Rachael. Assessment of positive emotion in horses: a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Veterinary Science at Massey University, Manawatū, New Zealand. (Doctoral dissertation, Massey University). (2022).
  126. Friard O, Gamba M. BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).
    doi: 10.1111/2041-210X.12584google scholar: lookup
  127. Reefmann N, BütikoferKaszàs F, Wechsler B, Gygax L. Ear and tail postures as indicators of emotional valence in sheep. Appl. Anim. Behav. Sci. 118, 199–207 (2009).
    doi: 10.1016/j.applanim.2009.02.013google scholar: lookup
  128. Harewood EJ, McGowan CM. Behavioral and physiological responses to stabling in naive horses. J. Equine Vet. Sci. 25, 164–170 (2005).
    doi: 10.1016/j.jevs.2005.03.008google scholar: lookup
  129. Garamszegi LZ. Comparing effect sizes across variables: Generalization without the need for Bonferroni correction. Behav. Ecol. 17, 682–687 (2006).
    doi: 10.1093/beheco/ark005google scholar: lookup
  130. Moran MD. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405 (2003).
    doi: 10.1034/j.1600-0706.2003.12010.xgoogle scholar: lookup
  131. Perneger TV. What’s wrong with Bonferroni adjustments. BMJ 316, 1236–1238 (1998).
    doi: 10.1136/bmj.316.7139.1236pmc: PMC1112991pubmed: 9553006google scholar: lookup

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