Skip to main content
SpringerLink
Log in

Visual laterality responses to different emotive stimuli by red-capped mangabeys, Cercocebus torquatus torquatus

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

Abstract

Hemispheric asymmetry in emotional perception has been put forward by different theories as the right hemisphere theory or the valence theory. But no consensus was found about the role played by both hemispheres. So, in order to test the different theories, we investigated preferential use of one eye in red-capped mangabeys, at the individual as well as at the group level. In this study we investigated the influence of the emotional value of stimuli on the direction and strength of visual preference of 14 red-capped mangabeys. Temporal stability of the bias of use of a given eye was evaluated by comparing our current results to those obtained 2.5 months previously. Two experimental devices, a tube and a box, tested five different stimuli: four food types varying in palatability and a neutral stimulus. The subjects’ food preferences were evaluated before testing the laterality. The mangabeys used their left eyes predominantly at the group level for the tube task. The majority of the subjects showed a visual preference at the individual level for the box task, but this bias was not present at the group level. As the palatability of the stimuli increased, the number of lateralized subjects and the number of subjects using preferentially their left eye increased. Similarly, the strength of laterality was related to food preference. Strength of laterality was significantly higher for subjects using their left eye than for subjects using their right eye. Preferential use of a given eye was stable over short periods 2.5 months later. Our data agree with reports on visual laterality for other species. Our results support the valence theory of a hemispheric sharing of control of emotions in relation to their emotional value.

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

Similar content being viewed by others

References

  • Andrew RJ, Rogers LJ (2002) The nature of lateralization in tetrapods. In: Rogers LJ, Andrew RJ (eds) Comparative vertebrate lateralization. Cambridge University Press, Cambridge, pp 94–125

    Google Scholar 

  • Baraud I (2007) Interactions sociales et modalités sensorielles (vocale et visuelle) impliquées, chez deux espèces de mangabés (Cercocebus torquatus torquatus et Lophocebus albigena albigena). PhD thesis, University of Rennes, pp 59–90

  • 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 22:411–426

    Article  PubMed  CAS  Google Scholar 

  • Bishop PO, Jeremy D, Lance JW (1953) The optic nerve: properties of a central tract. J Physiol 121:415–432

    PubMed  CAS  Google Scholar 

  • Blois-Heulin C, Guitton JS, Nedellec-Bienvenue D, Ropars L, Vallet E (2006) Hand preference in unimanual and bimanual task and postural effect on manual laterality in captive red-capped mangabey (Cercocebus torquatus torquatus). Am J Primatol 68:1–16

    Article  Google Scholar 

  • Boles DB (1987) Reaction time asymmetry through bilateral versus unilateral stimulus presentation. Brain Cogn 6:321–333

    Article  PubMed  CAS  Google Scholar 

  • Borod JC (1992) Interhemispheric and intrahemispheric control of emotion: a focus on unilateral brain damage. J Consult Clin Psychol 60:339–348

    Article  PubMed  CAS  Google Scholar 

  • Bourassa DC, McManus IC, Bryden MP (1996) Handedness and eye-dominance: a meta-analysis of their relationship. Laterality 1:5–34

    Article  PubMed  CAS  Google Scholar 

  • Bourne VJ (2006) The divided visual field paradigm: methodological considerations. Laterality 11(4):373–393

    PubMed  Google Scholar 

  • Brown ER, Taylor P (1988) Handedness, footedness and eyedness. Percept Mot Skills 66:183–186

    PubMed  CAS  Google Scholar 

  • Cantalupo C, Ward JP (2000) Interaction between lateralized systems: exploring the complexity of laterality. Brain Cogn 43:73–78

    PubMed  CAS  Google Scholar 

  • Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralization of predator evasion response in a teleost fish (Girardinus falcatus: Poeciliidae). Neuropsychologia 33:1637–1646

    Article  PubMed  CAS  Google Scholar 

  • Casperd LM, Dunbar RIM (1996) Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons. Behav Processes 37:57–65

    Article  Google Scholar 

  • Chapelain AS, Blois-Heulin C (2008) Eye preference in Campbell’s monkeys (Cercopithecus c. campbelli). Anim Cogn

  • Chapelain AS, Bec P, Blois-Heulin C (2006) Manual laterality in Campbell’s monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions. Behav Brain Res 173:237–245

    Article  PubMed  Google Scholar 

  • Cole J (1957) Laterality in the use of the hand, foot and eye in monkeys. J Comp Physiol 50:296–299

    CAS  Google Scholar 

  • Dadda M, Sovrano V, Bisazza A (2003) Temporal pattern of social aggregation in tadpoles: an influence on the measurement of lateralised response to social stimuli. Physiol Behav 78:337–341

    Article  PubMed  CAS  Google Scholar 

  • Davidson RJ (1992) Emotion and affective style: hemispheric substrates. Psychol Sci 3:39–43

    Article  Google Scholar 

  • Deckel AW, Fuqua L (1998) Effects of serotonergic drugs on lateralized aggression and aggressive displays in Anolis carolinensis. Behav Brain Res 95:227–232

    Article  PubMed  CAS  Google Scholar 

  • Dépy D, Fagot J, Vauclair J (1998) Comparative assessment of distance processing and hemispheric specialization in humans (Homo sapiens) and baboons (Papio papio). Brain Cogn 38:165–182

    Article  PubMed  Google Scholar 

  • Deuel RK, Dunlop NL (1980) Hand preference in the rhesus monkey: implications for the study of cerebral dominance. Arch Neurol 37:217–221

    PubMed  CAS  Google Scholar 

  • Erhan H, Borod JC, Tenke CE, Bruder GE (1998) Identification of emotion in a dichotic listening task: event-related brain potential and behavioral findings. Brain Cogn 37:286–307

    Article  PubMed  CAS  Google Scholar 

  • Fagart J (2004) Que signifie d’être droitier (ou gaucher)? In: Fagart J (ed) Droitiers/Gauchers. Des asymétries dans tous les sens. Solal, pp 15–48

  • Fagot J, Vauclair J (1988) Handedness and manual specialization in the baboon. Neuropsychologia 26:795–804

    Article  PubMed  CAS  Google Scholar 

  • Franklin WE, Lima SL (2001) Laterality in avian vigilance; do sparrow have a favourite eye? Anim Behav 62:879–885

    Article  Google Scholar 

  • Gautier-Hion A, Colyn M, Gautier JP (1999) Histoire naturelle des primates d’Afrique centrale. ECOFAC, Libreville, pp 60–68

    Google Scholar 

  • Ghirlanda S, Vallortigara G (2004) The evolution of brain lateralization: a game theoretical analysis of population structure. Proc R Soc B 271:853–857

    Article  PubMed  Google Scholar 

  • Hamilton CR, Vermeire BA (1988) Complementary hemispheric specialization in monkeys. Science 242:1691–1694

    Article  PubMed  CAS  Google Scholar 

  • Hook-Costigan MA, Rogers LJ (1995) Hand, mouth and eye preferences in the common marmosets (Callithrix jacchus). Folia Primatol 64:180–191

    Article  PubMed  CAS  Google Scholar 

  • Hook-Costigan MA, Rogers LJ (1998) Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus and hand preferences. Laterality 3:109–130

    Article  PubMed  CAS  Google Scholar 

  • Hopkins WD, Bennett AJ (1994) Handedness and approach-avoiding behaviour in chimpanzees (Pan). J Exp Psychol Anim Behav Process 20:413–418

    Article  PubMed  CAS  Google Scholar 

  • Hopkins WD, Leavens DA (1998) Hand use and gestural communication in chimpanzees (Pan troglodytes). J Comp Psychol 112:95–99

    Article  PubMed  CAS  Google Scholar 

  • Hunter ZR, Brysbaert M (2008) Visual half-field experiments are a good measure of cerebral language dominance if used properly: evidence from fMRI. Neuropsychologia 46:316–325

    Article  PubMed  Google Scholar 

  • Kounin JS (1938) Laterality in monkeys. J Genet Psychol 52:375–393

    Google Scholar 

  • Kruper DC, Boyle BE, Patton RA (1966) Eyes and hand preferences in rhesus monkeys (Macaca mulatta). Psychon Sci 5:277–278

    Google Scholar 

  • Levy J (1977) The mammalian brain and the adaptive advantage of cerebral asymmetry. Ann NY Acad Sci 299:264–272

    Article  PubMed  CAS  Google Scholar 

  • Lippolis G, Bisazza A, Rogers LJ, Vallortigara G (2002) Lateralization of predator avoidance responses in three species of toads. Laterality 7:163–183

    PubMed  Google Scholar 

  • MacFerran J (1992) Head-cocking and visual exploration in cotton-top tamarins. Honors thesis, University of Sterling

  • Marchant LF, McGrew WC (1991) Laterality of function in apes: a meta-analysis of methods. J Hum Evol 21:425–438

    Article  Google Scholar 

  • McGrew WC, Marchant LF (1997) On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearb Phys Anthropol 40:201–232

    Article  Google Scholar 

  • Meunier H, Vauclair J (2007) Hand preferences on unimanual and bimanual tasks in white-faced capuchins (Cebus capucinus). Am J Primatol 69:1–6

    Article  Google Scholar 

  • Nasrallah HA, MacCalley-Whitters M, Kuperman M (1982) Neurological differences between paranoid and non-paranoid schizophrenia I: sensory-motor lateralization. J Clin Psychiatry 42:305–306

    Google Scholar 

  • Nedellec-Bienvenue D, Blois-Heulin C (2005) Eye preferences in red-capped mangabeys. Folia Primatol 76:234–237

    Article  PubMed  CAS  Google Scholar 

  • Plotnik J, Nelson PA, De Waal FBM (2003) Visual field information in the face perception of chimpanzees (Pan troglodytes). Ann NY Acad Sci 1000:94–98

    Article  PubMed  Google Scholar 

  • Quaranta A, Siniscalchi M, Vallortigara G (2007) Asymmetric tail-wagging responses by dogs to different emotive stimuli. Curr Biol 17:199–201

    Article  CAS  Google Scholar 

  • Resnick SM, Lazar J, Gur RE, Gur RC (1994) The stability of tachistoscopique measures of hemispheric specialization. Neuropsychologia 32:1419–1430

    Article  PubMed  CAS  Google Scholar 

  • Robins A, Lippolis G, Bisazza A, Vallortigara G, Rogers LJ (1998) Lateralized agonistic responses and hindlimb use in toads. Anim Behav 56:875–881

    Article  PubMed  Google Scholar 

  • Rogers LJ (1989) Laterality in animals. Int J Comp Psychol 3:5–25

    Google Scholar 

  • Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253

    Article  PubMed  CAS  Google Scholar 

  • Rogers LJ, Ward JP, Stafford D (1994) Eye dominance in the small-eared bushbaby, Otolemeur garnetti. Neuropsychologia 32:257–264

    Article  PubMed  CAS  Google Scholar 

  • Rogers LJ, Zucca P, Vallortigara G (2004) Advantage of having a lateralized brain. Proc R Soc Lond B 271:S420–S422

    Article  Google Scholar 

  • Sovrano VA, Rainoldi C, Bisazza A, Vallortigara G (1999) Roots of brain specializations: preferential let-eye use during mirror-image inspection in six species of teleost fish. Behav Brain Res 106:175–180

    Article  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2001) Lateralization of response to social stimuli in fishes: a comparison between different methods and species. Physiol Behav 74:237–244

    Article  PubMed  CAS  Google Scholar 

  • Trouillard E, Blois-Heulin C (2005) Manual laterality and task complexity in De Brazza’s monkey (Cercopithecus neglectus). Laterality 10:7–27

    PubMed  Google Scholar 

  • Vallortigara G (2000) Comparative neuropsychology of the dual brain: a stroll through the left and right animals’ perceptual worlds. Brain Lang 73:189–219

    Article  PubMed  CAS  Google Scholar 

  • Vallortigara G (2006) The evolutionary psychology of left and right: costs and benefits of lateralization. Dev Psychobiol 48:418–427

    Article  PubMed  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 

  • Vallortigara G, Regolin L, Pagni P (1999a) Detour behaviour, imprinting, and visual lateralization in the domestic chick. Cogn Brain Res 7:307–320

    Article  CAS  Google Scholar 

  • Vallortigara G, Rogers LJ, Bisazza A (1999b) Possible evolutionary origins of cognitive brain lateralization. Brain Res Rev 30:164–175

    Article  PubMed  CAS  Google Scholar 

  • Vauclair J, Fagot J (1987) Spontaneous hand usage and handedness in a troop of baboons. Cortex 23:265–274

    PubMed  CAS  Google Scholar 

  • Vauclair J, Meguerditchian A, Hopkins WD (2005) Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Cogn Brain Res 25:210–216

    Article  Google Scholar 

  • Ventolini N, Ferrero EA, Sponza S, Della Chiesas A, Zucca P, Vallortigara G (2005) Laterality in the wild: preferential hemifield use during predatory and sexual behaviour in the black winged stilt (Himantopus himantopus). Anim Behav 69:1077–1084

    Article  Google Scholar 

  • Vermeire BA, Hamilton CR (1998) Inversion effect for faces in split-brain monkeys. Neuropsychologia 36:1003–1014

    Article  PubMed  CAS  Google Scholar 

  • Vermeire BA, Hamilton CR, Erdmann AL (1998) Right-hemispheric superiority in split-brain monkeys for learning and remembering facial discriminations. Behav Neurosci 112:1048–1061

    Article  PubMed  CAS  Google Scholar 

  • Warren JM (1980) Handedness and laterality in humans and other animals. Physiol Psychol 8:351–359

    Google Scholar 

  • Westergaard GC, Suomi SJ (1996) Hand preference for bimanual task in tufted capuchins (Cebus paella) and rhesus macaques (Macaca mulatta). J Comp Psychol 110:406–411

    Article  PubMed  CAS  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 44:13–20

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Ann Cloarec for helpful comments and translation of the manuscript and the three anonymous reviewers for interesting comments. The experiments comply with the current French laws.

Author information

Authors and Affiliations

  1. UMR CNRS 6552, Université de Rennes 1, Station Biologique, 35380, Paimpont, France

    Marion de Latude, Marianne Demange, Philippe Bec & Catherine Blois-Heulin

  2. UMR CNRS/uB 5561 Biogéosciences, Université de Bourgogne, Dijon, France

    Marion de Latude

Authors
  1. Marion de Latude
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marianne Demange
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Bec
    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

Corresponding author

Correspondence to Catherine Blois-Heulin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Latude, M., Demange, M., Bec, P. et al. Visual laterality responses to different emotive stimuli by red-capped mangabeys, Cercocebus torquatus torquatus . Anim Cogn 12, 31–42 (2009). https://doi.org/10.1007/s10071-008-0166-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-008-0166-z

Keywords

Search

Navigation