Advertisement

What do wild saiga antelopes tell us about the relative roles of the two brain hemispheres in social interactions?

  • Andrey Giljov
  • Yegor Malashichev
  • Karina KareninaEmail author
Original Paper

Abstract

Two brain hemispheres are unequally involved in the processing of social stimuli, as demonstrated in a wide range of vertebrates. A considerable number of studies have shown the right hemisphere advantage for social processing. At the same time, an approach–withdrawal hypothesis, mainly based on experimental evidence, proposes the involvement of both brain hemispheres according to approach and withdrawal motivation. The present study aimed to test the relative roles of the two hemispheres in social responses displayed in a natural context. Visual biases, implicating hemispheric lateralization, were estimated in the social interactions of saiga antelope in the wild. In individually identified males, the left/right visual field use during approach and withdrawal responses was recorded based on the lateral head/body position, relative to the conspecific. Lateralized approach responses were investigated in three types of interactions, with left visual field bias found for chasing a rival, no bias—for attacking a rival, and right visual field bias—for pursuing a female. In two types of withdrawal responses, left visual field bias was found for retreating after fighting, while no bias was evident in fight rejecting. These findings demonstrate that neither the right hemisphere advantage nor the approach–withdrawal distinction can fully explain the patterns of lateralization observed in social behaviour. It is clear that both brain hemispheres play significant roles in social responses, while their relative contribution is likely determined by a complex set of motivational and emotional factors rather than a simple dichotomous distinction such as, for example, approach versus withdrawal motivation.

Keywords

Laterality Hemispheric specialization Brain asymmetry Eye preference Ungulate Contest behaviour 

Notes

Acknowledgements

We are grateful to Anna Lushchekina and the staff of Stepnoi State Nature Sanctuary, and especially Vladimir Kalmykov, for valuable support and assistance during data collection.

Funding

This work was supported by the Russian Science Foundation (Grant No. 14-14-00284).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in the study were in accordance with the ethical standards of the St. Petersburg State University ethical committee (Permit No. 131-03-4).

Informed consent

Informed consent is not applicable to the study since no human subjects were included in the study.

Supplementary material

10071_2019_1259_MOESM1_ESM.pdf (685 kb)
Supplementary material 1 (PDF 684 kb) Online Resource. Output of binary logistic regression model used to analyze possible associations of visual field use (dependent variable) with the type of interaction, males’ age and year of study (independent variables).

References

  1. Altman J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267.  https://doi.org/10.1163/156853974X00534 CrossRefGoogle Scholar
  2. Austin NP, Rogers LJ (2012) Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Anim Behav 83:239–247.  https://doi.org/10.1016/j.anbehav.2011.10.033 CrossRefGoogle Scholar
  3. Austin NP, Rogers LJ (2014) Lateralization of agonistic and vigilance responses in Przewalski’s horses (Equus przewalskii). Appl Anim Behav Sci 151:43–50.  https://doi.org/10.1016/j.applanim.2013.11.011 CrossRefGoogle Scholar
  4. Baraud I, Buytet B, Bec P, Blois-Heulin C (2009) Social laterality and ‘transversality’in two species of mangabeys: influence of rank and implication for hemispheric specialization. Behav Brain Res 198(2):449–458.  https://doi.org/10.1016/j.bbr.2008.11.032 CrossRefGoogle Scholar
  5. Bekenov AB, Grachev IA, Milner-Gulland EJ (1998) The ecology and management of the saiga antelope in Kazakhstan. Mamm Rev 28(1):1–52.  https://doi.org/10.1046/j.1365-2907.1998.281024.x CrossRefGoogle Scholar
  6. Bordes CN, Ceacero F, Kotrba R (2018) Cues and mechanisms for lateral exposure preference in the common eland (Taurotragus oryx). Behav Ecol Sociobiol 72(7):120.  https://doi.org/10.1007/s00265-018-2535-1 CrossRefGoogle Scholar
  7. Brancucci A, Lucci G, Mazzatenta A, Tommasi L (2009) Asymmetries of the human social brain in the visual, auditory and chemical modalities. Philos Trans R Soc Lond B Biol Sci 364:895–914.  https://doi.org/10.1098/rstb.2008.0279 CrossRefGoogle Scholar
  8. Bullock SP, Rogers LJ (1992) Hemispheric specialization for the control of copulation in the young chick and effects of 5α-dihydrotestosterone and 17β-oestradiol. Behav Brain Res 48(1):9–14.  https://doi.org/10.1016/S0166-4328(05)80133-0 CrossRefGoogle Scholar
  9. Calvo MG, Rodríguez-Chinea S, Fernández-Martín A (2015) Lateralized discrimination of emotional scenes in peripheral vision. Exp Brain Res 233(3):997–1006.  https://doi.org/10.1007/s00221-014-4174-8 CrossRefGoogle Scholar
  10. Camerlink I, Menneson S, Turner SP, Farish M, Arnott G (2018) Lateralization influences contest behaviour in domestic pigs. Sci Rep 8:12116CrossRefGoogle Scholar
  11. Farmer K, Krüger K, Byrne RW, Marr I (2018) Sensory laterality in affiliative interactions in domestic horses and ponies (Equus caballus). Anim Cogn 21(5):631–637.  https://doi.org/10.1007/s10071-018-1196-9 CrossRefGoogle Scholar
  12. Forrester GS, Todd BK (2018) A comparative perspective on lateral biases and social behavior. In: Forrester GS, Hopkins WD, Hudry K, Lindell A (eds) Progress in brain research. Cerebral lateralization and cognition: evolutionary and developmental investigations of behavioral biases, vol 238. Elsevier, New York, pp 377–403.  https://doi.org/10.1016/bs.pbr.2018.06.014 CrossRefGoogle Scholar
  13. Forrester GS, Crawley M, Palmer C (2014) Social environment elicits lateralized navigational paths in two populations of typically developing children. Brain Cogn 91:21–27.  https://doi.org/10.1016/j.bandc.2014.07.005 CrossRefGoogle Scholar
  14. Ghirlanda S, Vallortigara G (2004) The evolution of brain lateralization: a game-theoretical analysis of population structure. Proc R Soc Lond B Biol Sci 271:853–857.  https://doi.org/10.1098/rspb.2003.2669 CrossRefGoogle Scholar
  15. Ghirlanda S, Frasnelli E, Vallortigara G (2009) Intraspecific competition and coordination in the evolution of lateralization. Philos Trans R Soc Lond B Biol Sci 364:861–866.  https://doi.org/10.1098/rstb.2008.0227 CrossRefGoogle Scholar
  16. Gilev A, Karenina K (2015) The significance of artesian wells for saigas within the Stepnoi Sanctuary, Astrakhan region. Saiga News 20:15–17Google Scholar
  17. Harmon-Jones E (2004) On the relationship of anterior brain activity and anger: examining the role of attitude toward anger. Cogn Emot 18:337–361.  https://doi.org/10.1080/02699930341000059 CrossRefGoogle Scholar
  18. Herron MA, Martin JE, Joyce JR (1978) Quantitative study of the decussating optic axons in the pony, cow, sheep, and pig. Am J Vet Res 39:1137–1139Google Scholar
  19. Howard KJ, Rogers LJ, Boura ALA (1980) Functional lateralization of the chicken forebrain revealed by use of intracranial glutamate. Brain Res 188(2):369–382.  https://doi.org/10.1016/0006-8993(80)90038-4 CrossRefGoogle Scholar
  20. Kaplan G (2017) Audition and hemispheric specialization in songbirds and new evidence from Australian magpies. Symmetry 9(7):99.  https://doi.org/10.3390/sym9070099 CrossRefGoogle Scholar
  21. Karenina K, Giljov A (2018) Mother and offspring lateralized social behavior across mammalian species. In: Forrester GS, Hopkins WD, Hudry K, Lindell A (eds) Progress in brain research. Cerebral lateralization and cognition: evolutionary and developmental investigations of behavioral biases, vol 238. Elsevier, New York, pp 115–141.  https://doi.org/10.1016/bs.pbr.2018.06.003 CrossRefGoogle Scholar
  22. Karenina KA, Giljov AN, Malashichev YB (2013) Eye as a key element of conspecific image eliciting lateralized response in fish. Anim Cogn 16(2):287–300.  https://doi.org/10.1007/s10071-012-0572-0 CrossRefGoogle Scholar
  23. Karenina K, Giljov A, Ingram J, Rowntree VJ, Malashichev Y (2017) Lateralization of mother–infant interactions in a diverse range of mammal species. Nat Ecol Evol 1:0030.  https://doi.org/10.1038/s41559-016-0030 CrossRefGoogle Scholar
  24. Karimova TY, Lushchekina AA (2018) Features of the spatial distribution and ethological structure of saiga population within the “Stepnoy” sanctuary (Astrakhan oblast). Ecosystems 2:73–91.  https://doi.org/10.24411/2542-2006-2017-10004 Google Scholar
  25. Kelley NJ, Hortensius R, Schutter DJ, Harmon-Jones E (2017) The relationship of approach/avoidance motivation and asymmetric frontal cortical activity: a review of studies manipulating frontal asymmetry. Int J Psychophysiol 119:19–30.  https://doi.org/10.1016/j.ijpsycho.2017.03.001 CrossRefGoogle Scholar
  26. Kiley-Worthington M, de la Plain S (1983) The cow’s world. The behaviour of beef suckler cattle (Bos Taurus). Tierhaltung/animal management, vol 14. Birkhäuser, Basel, pp 23–34.  https://doi.org/10.1007/978-3-0348-6782-5_2 CrossRefGoogle Scholar
  27. Koboroff A, Kaplan G, Rogers LJ (2008) Hemispheric specialization in Australian magpies (Gymnorhina tibicen) shown as eye preferences during response to a predator. Brain Res Bull 76(3):304–306.  https://doi.org/10.1016/j.brainresbull.2008.02.015 CrossRefGoogle Scholar
  28. Lindell AK (2013) Continuities in emotion lateralization in human and non-human primates. Front Hum Neurosci 7:464.  https://doi.org/10.3389/fnhum.2013.00464 CrossRefGoogle Scholar
  29. Milner-Gulland EJ (2001) A dynamic game model for the decision to join an aggregation. Ecol Model 145:85–99.  https://doi.org/10.1016/S0304-3800(01)00381-7 CrossRefGoogle Scholar
  30. Milner-Gulland EJ, Bukreeva OM, Coulson T, Lushchekina AA, Kholodova MV, Bekenov AB, Grachev IA (2003) Reproductive collapse in saiga antelope harems. Nature 422(6928):135.  https://doi.org/10.1038/422135a CrossRefGoogle Scholar
  31. Najt P, Bayer U, Hausmann M (2013) Models of hemispheric specialization in facial emotion perception—a reevaluation. Emotion 13(1):159–167.  https://doi.org/10.1037/a0029723 CrossRefGoogle Scholar
  32. Neronov VM, Arylova NY, Dubinin MY, Karimova TY, Lushchekina AA (2013) Current state and prospects of preserving saiga antelope in Northwest Pre-Caspian region. Arid Ecosyst 3(2):57–64.  https://doi.org/10.1134/s2079096113020078 CrossRefGoogle Scholar
  33. Peirce JW, Leigh AE, Kendrick KM (2000) Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia 38(4):475–483.  https://doi.org/10.1016/S0028-3932(99)00088-3 CrossRefGoogle Scholar
  34. Phillips CJC, Oevermans H, Syrett KL, Jespersen AY, Pearce GP (2015) Lateralization of behavior in dairy cows in response to conspecifics and novel persons. J Dairy Sci 98(4):2389–2400.  https://doi.org/10.3168/jds.2014-8648 CrossRefGoogle Scholar
  35. Prete G, Laeng B, Fabri M, Foschi N, Tommasi L (2015) Right hemisphere or valence hypothesis, or both? The processing of hybrid faces in the intact and callosotomized brain. Neuropsychologia 68:94–106.  https://doi.org/10.1016/j.neuropsychologia.2015.01.002 CrossRefGoogle Scholar
  36. Quaresmini C, Forrester GS, Spiezio C, Vallortigara G (2014) Social environment elicits lateralized behaviors in gorillas and chimpanzees. J Comput Psychol 128:276–284.  https://doi.org/10.1037/a0036355 CrossRefGoogle Scholar
  37. Racca A, Guo K, Meints K, Mills DS (2012) Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children. PLoS ONE 7(4):e36076.  https://doi.org/10.1371/journal.pone.0036076 CrossRefGoogle Scholar
  38. Rogers LJ (2002) Lateralization in vertebrates: its early evolution, general pattern, and development. Advances in the study of behavior, vol 31. Academic Press, New York, pp 107–161.  https://doi.org/10.1016/S0065-3454(02)80007-9 Google Scholar
  39. Rogers LJ (2017) Eye and ear preferences. In: Rogers LJ, Vallortigara G (eds) Lateralized brain functions—methods in human and non-human species. Springer, New York, pp 79–102CrossRefGoogle Scholar
  40. Rogers LJ, Vallortigara G, Andrew RJ (2013) Divided brains. The biology and behaviour of brain asymmetries. Cambridge University Press, New YorkCrossRefGoogle Scholar
  41. Rosa Salva O, Regolin L, Mascalzoni E, Vallortigara G (2012) Cerebral and behavioural asymmetries in animal social recognition. Comp Cogn Behav Rev 7:110–138.  https://doi.org/10.3819/ccbr.2012.70006 CrossRefGoogle Scholar
  42. Siniscalchi M, Ingeo S, Quaranta A (2018) Orienting asymmetries and physiological reactivity in dogs’ response to human emotional faces. Learn Behav.  https://doi.org/10.3758/s13420-018-0325-2 Google Scholar
  43. Sokolov VE, Zhirnov LV (1998) The Saiga: phylogeny, systematics, ecology, conservation and use [filogeniya, sistematika, ekologiya, oxrana i ispol’zovanie]. Russian Academy of Sciences, Moscow (in Russian) Google Scholar
  44. Teer JG, Neronov VM, Zhirnov LV, Blizniuk AI (1996) Status and exploitation of saiga antelope in Kalmykia. In: Taylor VJ, Dunstone N (eds) The exploitation of mammal populations. Chapman and Hall, London, pp 75–87.  https://doi.org/10.1007/978-94-009-1525-1 CrossRefGoogle Scholar
  45. Thomas NA, Wignall SJ, Loetscher T, Nicholls ME (2014) Searching the expressive face: evidence for both the right hemisphere and valence-specific hypotheses. Emotion 14(5):962.  https://doi.org/10.1037/a0037033 CrossRefGoogle Scholar
  46. Underwood R (1982) Vigilance behaviour in grazing African antelopes. Behaviour 79(2):81–107.  https://doi.org/10.1163/156853982X00193 CrossRefGoogle Scholar
  47. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589.  https://doi.org/10.1017/S0140525X05000105 Google Scholar
  48. Vallortigara G, Versace E (2017) Laterality at the neural, cognitive, and behavioral levels. In: Call J (ed) APA Handbook of comparative psychology, vol 1. Basic concepts, methods, neural substrate, and behavior. American Psychological Association, Washington DC, pp 557–577Google Scholar
  49. Vauclair J, Yamazaki Y, Güntürkün O (2006) The study of hemispheric specialization for categorical and coordinate spatial relations in animals. Neuropsychologia 44:1524–1534.  https://doi.org/10.1016/j.neuropsychologia.2006.01.021 CrossRefGoogle Scholar
  50. Ventolini N, Ferrero EA, Sponza S, Della Chiesa A, Zucca P, Vallortigara G (2005) Laterality in the wild: preferential hemifield use during predatory and sexual behavior in the black-winged stilt. Anim Behav 69:1077–1084.  https://doi.org/10.1016/j.anbehav.2004.09.003 CrossRefGoogle Scholar
  51. Versace E, Morgante M, Pulina G, Vallortigara G (2007) Behavioural lateralization in sheep (Ovis aries). Behav Brain Res 184:72–80.  https://doi.org/10.1016/j.bbr.2007.06.016 CrossRefGoogle Scholar
  52. Wedding D, Stalans L (1985) Hemispheric differences in the perception of positive and negative faces. Int J Neurosci 27:277–281.  https://doi.org/10.3109/00207458509149773 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Vertebrate Zoology, Faculty of BiologySaint Petersburg State UniversitySaint PetersburgRussia
  2. 2.Laboratory of Molecular Neurobiology, Department of Ecological PhysiologyInstitute of Experimental MedicineSaint PetersburgRussia

Personalised recommendations