Skip to main content
SpringerLink
Log in

Socially dependent auditory laterality in domestic horses (Equus caballus)

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andrew RJ (1974) Arousal and the causation of behaviour. Behaviour 51(3–4):135–164

    Article  PubMed  CAS  Google Scholar 

  • 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 94–125

    Google Scholar 

  • 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 363–365

    Google Scholar 

  • Austin NP, Rogers LJ (2007) Asymmetry of flight and escape turning responses in horses. Laterality 12(5):464–474. doi:10.1080/13576500701495307

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):411–426

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 6:330–357

    Google Scholar 

  • 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 9:227–238

    Article  CAS  Google Scholar 

  • Burton F (2000) The horse’s world. In: McEwen J (ed) Ultimate horse care. Ringpress Book Ltd, Sydney, pp 140–162

    Google Scholar 

  • Corballis MC (2008) Of mice and men––and lopsided birds. Cortex 44:3–7

    Article  PubMed  Google Scholar 

  • Csermely D (2004) Lateralisation in birds of prey: adaptive and phylogenetic considerations. Behav Process 67:511–520

    Article  Google Scholar 

  • Cynx J, Williams H, Nottebohm F (1992) Hemispheric differences in avian song discrimination. Proc Natl Acad Sci USA 89:1372–1375

    Article  PubMed  CAS  Google Scholar 

  • 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 94:487–490

    Article  PubMed  CAS  Google Scholar 

  • 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):31–42

    Article  PubMed  Google Scholar 

  • Deng C, Rogers LJ (2002) Social recognition and approach in the chick: lateralization and effect of visual experience. Anim behav 63:697–706

    Article  Google Scholar 

  • 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 83–93

    Google Scholar 

  • Friederici AD, Alter K (2004) Lateralization of auditory language functions: a dynamic dual pathway model. Brain Lang 89:267–276

    Article  PubMed  Google Scholar 

  • George I, Cousillas H, Richard J-P, Hausberger M (2002) Song perception in the European starling: hemispheric specialization and individual variations. CR Biol 325:197–204

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • George I, Cousillas H, Richard JP, Hausberger M (2005) State-dependent hemispheric specialization in the songbird brain. J Comp Neurol 488:48–60

    Article  PubMed  Google Scholar 

  • 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 58:163–172

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Hauser MD (1993) Right hemisphere dominance for the production of facial expression in monkeys. Science 261:475–477

    Article  PubMed  CAS  Google Scholar 

  • 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 91:3946–3948

    Article  PubMed  CAS  Google Scholar 

  • Hauser MD, Agnetta B, Perez C (1998) Orienting asymmetries in rhesus monkeys: the effect of time-domain changes on acoustic perception. Anim behav 56:41–47

    Article  PubMed  Google Scholar 

  • Heffner HE, Heffner RS (1989) Unilateral auditory cortex ablation in macaques results in a contralateral hearing loss. J Neurophysiol 62:789

    PubMed  CAS  Google Scholar 

  • 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 207–219

    Google Scholar 

  • Hugdahl K (2000a) Lateralization of cognitive processes in the brain. Acta Psychol 105:211–235

    Article  CAS  Google Scholar 

  • Hugdahl K (2000b) What can be learned about brain function from dichotic listening? Rev Esp Neuropsi 2(3):62–84

    Google Scholar 

  • 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 53:609–616

    Article  PubMed  Google Scholar 

  • Kimura D (1967) Functional asymmetry of the brain in dichotic listening. Cortex 3:163–168

    Google Scholar 

  • Larose C, Richard-Yris MA, Hausberger M, Rogers LJ (2006) Laterality of horses associated with emotionality in novel situations. Laterality 11(4):355–367

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mc Greevy PD, Thomson PC (2005) Differences in motor laterality between breeds of performance horse. Appl Anim Behav Sci 99:183–190

    Article  Google Scholar 

  • Mertl-Millhollen A (2007) Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs. Am J Primatol 69:635–640

    Article  PubMed  Google Scholar 

  • Murphy J, Sutherland A, Arkins S (2005) Idiosyncratic motor laterality in the horse. Appl Anim Behav Sci 91:297–310

    Article  Google Scholar 

  • Nealen PM, Schmidt FM (2002) Comparartive approaches to avian song system fonction: insights into auditory and motor processing. J Comp Physiol 188:929–941

    Article  CAS  Google Scholar 

  • Ödberg FO (1974) Some aspects of the acoustic expression in horses. In: Zeeb K (ed) Ethologie und Ökologie bei der Haustierhaltung. KTBL, Darmstadt, pp 89–105

    Google Scholar 

  • Ödberg FO (1978) A study of the hearing ability of horses. Equine Vet J 10(2):82–84

    Article  PubMed  Google Scholar 

  • Palleroni A, Hauser MD (2003) Experience-dependent plasticity for auditory processing in a raptor. Science 299(5610):1195

    Article  PubMed  CAS  Google Scholar 

  • Pell MD (2006) Cerebral mechanisms for understanding emotional prosody in speech. Brain Lang 96:221–234

    Article  PubMed  Google Scholar 

  • 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):324–327

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 427:448–451

    Article  PubMed  CAS  Google Scholar 

  • 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 94:197–206

    Article  PubMed  Google Scholar 

  • Richard JP (1991) Sound analysis and synthesis using an amiga micro-computer. Bioacoustics 3(1):45–60

    Google Scholar 

  • Robins A, Rogers LJ (2006) Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiol Learn Mem 86:214–227

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rosenzweig MR (1951) Representations of the two ears at the auditory cortex. Am J Physiol 167:147–214

    PubMed  CAS  Google Scholar 

  • Sato W, Aoki S (2006) Right hemispheric dominance in processing of unconscious negative emotion. Brain Cogn 62:261–266

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schmidt MF, Konishi M (1998) Gating of auditory responses in the vocal control system of awake songbirds. Nat Neurosci 1(6):513–518

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sommer IEC, Ramsey NF, Kahn RS (2001) Language lateralization in schizophrenia, an fMRI study. Schizophr Res 52:57–67

    Article  PubMed  CAS  Google Scholar 

  • Sommer IEC, Ramsey NF, Mandel RCW, Kahn RS (2003) Language lateralization in female patients with schizophrenia: an fMRI study. Schizophr Res 60:183–190

    Article  PubMed  CAS  Google Scholar 

  • Sovrano VA (2004) Visual lateralization in response to familiar and unfamiliar stimuli in fish. Behav Brain Res 152:385–391

    Article  PubMed  Google Scholar 

  • Taglialatela JP (2004) Functional asymmetries for bonobo vocal communication. PhD dissertation, Georgia State University

  • 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

    Article  Google Scholar 

  • Vallortigara G (1992) Right hemisphere advantage for social recognition in the chick. Neuropsychologia 30(9):761–768

    Article  PubMed  CAS  Google Scholar 

  • Vallortigara G, Andrew RJ (1991) Lateralization of response by chicks to change in a model partner. Anim Behav 41:187–194

    Article  Google Scholar 

  • Vallortigara G, Andrew RJ (1994) Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Process 33:41–58

    Article  Google Scholar 

  • Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589

    PubMed  Google Scholar 

  • Versace E, Morgante M, Pulina G, Vallortigara G (2007) Behavioural lateralization in sheep (Ovis aries). Behav Brain Res 184:72–80

    Article  PubMed  Google Scholar 

  • Waring GH (2003) Horse behaviour, 2nd edn. Noyes Publications/William Andrew Publishing, Norwich/New York, pp 18–299

    Google Scholar 

  • 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 91–145

  • 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 139:79–87

    Article  Google Scholar 

  • 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):13–20

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Université de Rennes I, EthoS, Ethologie animale et humaine-UMR 6552-CNRS Station Biologique de Paimpont, 35380, Paimpont, France

    Muriel Basile, Sarah Boivin, Anaïs Boutin, Catherine Blois-Heulin, Martine Hausberger & Alban Lemasson

Authors
  1. Muriel Basile
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Boivin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anaïs Boutin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine Blois-Heulin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martine Hausberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alban Lemasson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muriel Basile.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Basile, M., Boivin, S., Boutin, A. et al. Socially dependent auditory laterality in domestic horses (Equus caballus). Anim Cogn 12, 611–619 (2009). https://doi.org/10.1007/s10071-009-0220-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-009-0220-5

Keywords

Search

Navigation