Animal Cognition

, Volume 12, Issue 4, pp 611–619 | Cite as

Socially dependent auditory laterality in domestic horses (Equus caballus)

  • Muriel BasileEmail author
  • Sarah Boivin
  • Anaïs Boutin
  • Catherine Blois-Heulin
  • Martine Hausberger
  • Alban Lemasson
Original Paper


Laterality is now known to be an ubiquitous phenomenon among the vertebrates. Particularly, laterality of auditory processing has been demonstrated in a variety of species, especially songbirds and primates. Such a hemispheric specialization has been shown to depend on factors such as sound structure, species specificity and types of stimuli. Much less is known on the possible influence of social familiarity although a few studies suggest such an influence. Here we tested the influence of the degree of familiarity on the laterality of the auditory response in the domestic horse. This species is known for its social system and shows visible reactions to sounds, with one or two ears moving towards a sound source. By comparing such responses to the playback of different conspecific whinnies (group member, neighbor and stranger), we could demonstrate a clear left hemisphere (LH) preference for familiar neighbor calls while no preference was found for group member and stranger calls. Yet, we found an opposite pattern of ear side preference for neighbor versus stranger calls. These results are, to our knowledge, the first to demonstrate auditory laterality in an ungulate species. They open further lines of thought on the influence of the social “value” of calls and the listener’s arousal on auditory processing and laterality.


Auditory processing Behavioral asymmetry Vocalization Social familiarity Playback Attention 



This work was conducted at the “Laboratoire EthoS Ethologie animale et humaine”, at the Station Biologique de Paimpont, in France. We are especially grateful to the personnel and direction of the Lycée agricole La Touche de Ploërmel, the Lycée agricole de Laval for their interest and cooperation during this study. We are particularly thankful to Pascaline Le Gouar for useful advice, help and assistance on statistical analyses. We would also like to thank Richard Jean-Pierre, Samuel Gornet, Haïfa Benhajahali, Carole Fureix, for their technical assistance and help and George Morton for English corrections. We are particularly grateful to anonymous reviewers and the editor for their helpful comments and advice on this manuscript. The experiments complied with the current French laws governing animal research.


  1. Andrew RJ (1974) Arousal and the causation of behaviour. Behaviour 51(3–4):135–164PubMedCrossRefGoogle Scholar
  2. Andrew RJ, Rogers LJ (2002) The nature of lateralization in tetrapods. In: Rogers LJ, Andrew RJ (eds) Comparative vertebrate lateralization. Cambridge University Press, London, pp 94–125Google Scholar
  3. Andrew RJ, Watkins JAS (2002) Evidence for cerebral lateralization from senses other than vision. In: Rogers LJ, Andrew RJ (eds) Comparative vertebrate lateralization. Cambridge University Press, London, pp 363–365Google Scholar
  4. Austin NP, Rogers LJ (2007) Asymmetry of flight and escape turning responses in horses. Laterality 12(5):464–474. doi: 10.1080/13576500701495307 PubMedGoogle Scholar
  5. 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. doi: 10.1016/j.bbr.2008.11.032 PubMedCrossRefGoogle Scholar
  6. Bisazza A, Rogers LJ, Vallortigara G (1998) The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neurosci Biobehav Rev 22(3):411–426PubMedCrossRefGoogle Scholar
  7. Böye M, Güntürkün O, Vauclair J (2005) Right ear advantage for conspecific calls in adults and subadults, but not infants, California sea lions (Zalophus californianus): hemispheric specialization for communication? Eur J Neurosci 21(6):1727–1732. doi: 10.1111/1460-9568.2005.04005.x PubMedCrossRefGoogle Scholar
  8. Broca P (1861) Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bulletin de la Société Anatomique 6:330–357Google Scholar
  9. Buchanan TW, Lutz K, Mirzazade S, Specht K, Shah NJ, Zilles K, Jäncke L (2000) Recognition of emotional prosody and verbal components of spoken language: an fMRI study. Cogn Brain Res 9:227–238CrossRefGoogle Scholar
  10. Burton F (2000) The horse’s world. In: McEwen J (ed) Ultimate horse care. Ringpress Book Ltd, Sydney, pp 140–162Google Scholar
  11. Corballis MC (2008) Of mice and men––and lopsided birds. Cortex 44:3–7PubMedCrossRefGoogle Scholar
  12. Csermely D (2004) Lateralisation in birds of prey: adaptive and phylogenetic considerations. Behav Process 67:511–520CrossRefGoogle Scholar
  13. Cynx J, Williams H, Nottebohm F (1992) Hemispheric differences in avian song discrimination. Proc Natl Acad Sci USA 89:1372–1375PubMedCrossRefGoogle Scholar
  14. De Boyer Des Roches A, Richard-Yris MA, Henry S, Ezzaouïa M, Hausberger M (2008) Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects’ emotional value. Physiol Behav 94:487–490PubMedCrossRefGoogle Scholar
  15. De Latude M, Demange M, Bec P, Blois-Heulin C (2009) Visual laterality responses to different emotive stimuli by red-capped mangabeys, Cercocebus torquatus torquatus. Anim Cogn 12(1):31–42PubMedCrossRefGoogle Scholar
  16. Deng C, Rogers LJ (2002) Social recognition and approach in the chick: lateralization and effect of visual experience. Anim behav 63:697–706CrossRefGoogle Scholar
  17. Feh C (2005) Relationships and communication in socially natural horse herds. In: Mills DS, McDonnell SM (eds) The domestic horse: the origins, development and management of its behaviour. Cambridge University Press, London, pp 83–93Google Scholar
  18. Friederici AD, Alter K (2004) Lateralization of auditory language functions: a dynamic dual pathway model. Brain Lang 89:267–276PubMedCrossRefGoogle Scholar
  19. George I, Cousillas H, Richard J-P, Hausberger M (2002) Song perception in the European starling: hemispheric specialization and individual variations. CR Biol 325:197–204CrossRefGoogle Scholar
  20. George I, Vernier B, Richard JP, Hausberger M, Cousillas H (2004) Hemispheric specialization in the primary auditory area of awake and anesthetized starlings (Sturnus vulgaris). Behav Neurosci 118(3):597–610. doi: 10.1037/0735-7044.118.3.597 PubMedCrossRefGoogle Scholar
  21. George I, Cousillas H, Richard JP, Hausberger M (2005) State-dependent hemispheric specialization in the songbird brain. J Comp Neurol 488:48–60PubMedCrossRefGoogle Scholar
  22. Ghazanfar AA, Smith-Rohrberg D, Hauser MD (2001) The role of temporal cues in rhesus monkey vocal recognition: orienting asymmetries to reversed calls. Brain Behav Evol 58:163–172PubMedCrossRefGoogle Scholar
  23. Gil-da-Costa R, Hauser MD (2006) Vervet monkeys and humans show brain asymmetries for processing conspecific vocalizations, but with opposite patterns of laterality. Proc Biol Sci 273(1599):2313–2318. doi: 10.1098/rspb.2006.3580 PubMedCrossRefGoogle Scholar
  24. Hauser MD (1993) Right hemisphere dominance for the production of facial expression in monkeys. Science 261:475–477PubMedCrossRefGoogle Scholar
  25. Hauser MD, Andersson K (1994) Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: field experiments. Proc Natl Acad Sci USA 91:3946–3948PubMedCrossRefGoogle Scholar
  26. Hauser MD, Agnetta B, Perez C (1998) Orienting asymmetries in rhesus monkeys: the effect of time-domain changes on acoustic perception. Anim behav 56:41–47PubMedCrossRefGoogle Scholar
  27. Heffner HE, Heffner RS (1989) Unilateral auditory cortex ablation in macaques results in a contralateral hearing loss. J Neurophysiol 62:789PubMedGoogle Scholar
  28. Heffner HE, Heffner RS (1995) Role of auditory cortex in the perception of vocalizations by Japanese macaques. In: Zimmermann E et al (eds) Current topics in primate vocal communication. Plenum Press, New York, pp 207–219Google Scholar
  29. Hugdahl K (2000a) Lateralization of cognitive processes in the brain. Acta Psychol 105:211–235CrossRefGoogle Scholar
  30. Hugdahl K (2000b) What can be learned about brain function from dichotic listening? Rev Esp Neuropsi 2(3):62–84Google Scholar
  31. Hugdahl K, Rishovd Rund B, Lund A, Asbjørnsen A, Egeland J, Inge Landrø N, Roness A, Stordal KI, Sundet K (2003) Attentional and executive dysfunctions in schizophrenia and depression: evidence from dichotic listening performance. Biol psychiatry 53:609–616PubMedCrossRefGoogle Scholar
  32. Kimura D (1967) Functional asymmetry of the brain in dichotic listening. Cortex 3:163–168Google Scholar
  33. Larose C, Richard-Yris MA, Hausberger M, Rogers LJ (2006) Laterality of horses associated with emotionality in novel situations. Laterality 11(4):355–367PubMedGoogle Scholar
  34. Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV (2006) Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 16:1471–1476. doi: 10.1016/j.cub.2006.05.060 PubMedCrossRefGoogle Scholar
  35. Mc Greevy PD, Thomson PC (2005) Differences in motor laterality between breeds of performance horse. Appl Anim Behav Sci 99:183–190CrossRefGoogle Scholar
  36. Mertl-Millhollen A (2007) Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs. Am J Primatol 69:635–640PubMedCrossRefGoogle Scholar
  37. Murphy J, Sutherland A, Arkins S (2005) Idiosyncratic motor laterality in the horse. Appl Anim Behav Sci 91:297–310CrossRefGoogle Scholar
  38. Nealen PM, Schmidt FM (2002) Comparartive approaches to avian song system fonction: insights into auditory and motor processing. J Comp Physiol 188:929–941CrossRefGoogle Scholar
  39. Ödberg FO (1974) Some aspects of the acoustic expression in horses. In: Zeeb K (ed) Ethologie und Ökologie bei der Haustierhaltung. KTBL, Darmstadt, pp 89–105Google Scholar
  40. Ödberg FO (1978) A study of the hearing ability of horses. Equine Vet J 10(2):82–84PubMedCrossRefGoogle Scholar
  41. Palleroni A, Hauser MD (2003) Experience-dependent plasticity for auditory processing in a raptor. Science 299(5610):1195PubMedCrossRefGoogle Scholar
  42. Pell MD (2006) Cerebral mechanisms for understanding emotional prosody in speech. Brain Lang 96:221–234PubMedCrossRefGoogle Scholar
  43. Petersen MR, Beecher MD, Zoloth SR, Moody DB, Stebbins WC (1978) Neural lateralization of species-specific vocalizations by Japanese macaques (Macaca fuscata). Science 202(4365):324–327CrossRefGoogle Scholar
  44. Petkov CI, Kayser C, Steudel T, Whittingstall K, Augath M, Logothetis NK (2008) A voice region in the monkey brain. Nat Neurosci 11(3):367–374. doi: 10.1038/nn2043 PubMedCrossRefGoogle Scholar
  45. Poremba A, Malloy M, Saunders RC, Carson RE, Herscovitch P, Mishkin M (2004) Species-specific calls evoke asymmetric activity in the monkey’s temporal poles. Nature 427:448–451PubMedCrossRefGoogle Scholar
  46. Razafimandimby A, Maïza O, Hervé P-Y, Lecardeur L, Delamillieure P, Brazo P, Mazoyer B, Tzourio-Mazoyer N, Dollfus S (2007) Stability of functional language lateralization over time in schizophrenia patients. Schizophr Res 94:197–206PubMedCrossRefGoogle Scholar
  47. Richard JP (1991) Sound analysis and synthesis using an amiga micro-computer. Bioacoustics 3(1):45–60Google Scholar
  48. Robins A, Rogers LJ (2006) Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiol Learn Mem 86:214–227PubMedCrossRefGoogle Scholar
  49. Rogers LJ, Vallortigara G (2008) From antenna to antenna: lateral shift of olfactory memory in honeybees. PLoS ONE 3(6):e2340. doi: 10.1371/0002340 PubMedCrossRefGoogle Scholar
  50. Rosenzweig MR (1951) Representations of the two ears at the auditory cortex. Am J Physiol 167:147–214PubMedGoogle Scholar
  51. Sato W, Aoki S (2006) Right hemispheric dominance in processing of unconscious negative emotion. Brain Cogn 62:261–266PubMedCrossRefGoogle Scholar
  52. Scheumann M, Zimmermann E (2008) Sex-specific asymmetries in communication sound perception are not related to hand preference in an early primate. BMC Biol 6:3. doi: 10.1186/1741-7007-6-3 PubMedCrossRefGoogle Scholar
  53. Schmidt MF, Konishi M (1998) Gating of auditory responses in the vocal control system of awake songbirds. Nat Neurosci 1(6):513–518PubMedCrossRefGoogle Scholar
  54. Siniscalchi M, Quaranta A, Rogers LJ (2008) Hemispheric specialization in dogs for processing different acoustic stimuli. PloS ONE 3(10):e3349. doi: 10.1371/0003349 PubMedCrossRefGoogle Scholar
  55. Sommer IEC, Ramsey NF, Kahn RS (2001) Language lateralization in schizophrenia, an fMRI study. Schizophr Res 52:57–67PubMedCrossRefGoogle Scholar
  56. Sommer IEC, Ramsey NF, Mandel RCW, Kahn RS (2003) Language lateralization in female patients with schizophrenia: an fMRI study. Schizophr Res 60:183–190PubMedCrossRefGoogle Scholar
  57. Sovrano VA (2004) Visual lateralization in response to familiar and unfamiliar stimuli in fish. Behav Brain Res 152:385–391PubMedCrossRefGoogle Scholar
  58. Taglialatela JP (2004) Functional asymmetries for bonobo vocal communication. PhD dissertation, Georgia State UniversityGoogle Scholar
  59. Teufel C, Hammerschmidt K, Fischer J (2007) Lack of orienting asymmetries in Barbary macaques: implications for studies of lateralized auditory processing. Anim Behav 73(2):249–255. doi: 10.1016/2006.04.011 CrossRefGoogle Scholar
  60. Vallortigara G (1992) Right hemisphere advantage for social recognition in the chick. Neuropsychologia 30(9):761–768PubMedCrossRefGoogle Scholar
  61. Vallortigara G, Andrew RJ (1991) Lateralization of response by chicks to change in a model partner. Anim Behav 41:187–194CrossRefGoogle Scholar
  62. Vallortigara G, Andrew RJ (1994) Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Process 33:41–58CrossRefGoogle Scholar
  63. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589PubMedGoogle Scholar
  64. Versace E, Morgante M, Pulina G, Vallortigara G (2007) Behavioural lateralization in sheep (Ovis aries). Behav Brain Res 184:72–80PubMedCrossRefGoogle Scholar
  65. Waring GH (2003) Horse behaviour, 2nd edn. Noyes Publications/William Andrew Publishing, Norwich/New York, pp 18–299Google Scholar
  66. Wernicke C (1874) Der aphasische symptomencomplex: eine psychologische studie auf anatomischer basis. In: Eggert GH (ed) Wernicke’s works on aphasia: a sourcebook and review, pp 91–145Google Scholar
  67. Wich SA, Assink PR, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (primates; Presbytis thomasi): the effect of familiarity. Behaviour 139:79–87CrossRefGoogle Scholar
  68. Zucca P, Sovrano VA (2008) Animal lateralization and social recognition: quails use their left visual hemifield when approaching a companion and their right visual hemifield when approaching a stranger. Cortex 44(1):13–20PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Muriel Basile
    • 1
    Email author
  • Sarah Boivin
    • 1
  • Anaïs Boutin
    • 1
  • Catherine Blois-Heulin
    • 1
  • Martine Hausberger
    • 1
  • Alban Lemasson
    • 1
  1. 1.Université de Rennes I, EthoS, Ethologie animale et humaine-UMR 6552-CNRS Station Biologique de PaimpontPaimpontFrance

Personalised recommendations