Skip to main content
Log in

Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta)

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

Abstract

Both human and nonhuman primates preferentially orient toward other individuals and follow gaze in controlled environments. Precisely where any animal looks during natural behavior, however, remains unknown. We used a novel telemetric gaze-tracking system to record orienting behavior of ringtailed lemurs (Lemur catta) interacting with a naturalistic environment. We here provide the first evidence that ringtailed lemurs, group-living prosimian primates, preferentially gaze towards other individuals and, moreover, follow other lemurs’ gaze while freely moving and interacting in naturalistic social and ecological environments. Our results support the hypothesis that stem primates were capable of orienting toward and following the attention of other individuals. Such abilities may have enabled the evolution of more complex social behavior and cognition, including theory of mind and language, which require spontaneous attention sharing. This is the first study to use telemetric eye-tracking to quantitatively monitor gaze in any nonhuman animal during locomotion, feeding, and social interaction. Moreover, this is the first demonstration of gaze following by a prosimian primate and the first to report gaze following during spontaneous interaction in naturalistic social environments.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allman J (1999) Evolving brains. Scientific American Library, New York

    Google Scholar 

  • Anderson JR, Mitchell RW (1999) Macaques but not lemurs co-orient visually with humans. Folia Primatol (Basel) 70(1):17–22

    Article  CAS  Google Scholar 

  • APA (1994) Autistic Disorder Criterion A1. Diagnostic and Statistical Manual of Mental Disorders, 4th Edn. American Psychiatric Association, Washington, p 66

  • Baron-Cohen S (1994) How to build a baby that can read minds: cognitive mechanisms in mindreading. Curr Psychol Cogn 13:513–552

    Google Scholar 

  • Bayliss AP, diPellegrino G, Tipper SP (2005) Sex differences in eye gaze and symbolic cueing of attention. Q J Exp Psychol A 58(4):631–650

    PubMed  Google Scholar 

  • Brauer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119(2):145–154

    Article  PubMed  Google Scholar 

  • Brothers L (1990) The neural basis of primate social communication. Motiv Emot 14(2):81–91

    Article  Google Scholar 

  • Bugnyar T, Stowe M, Heinrich B (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc Biol Sci 271(1546):1331–1336

    Article  PubMed  Google Scholar 

  • Butler RA (1954) Incentive conditions which influence visual exploration. J Exp Psychol 48:19–23

    Article  PubMed  CAS  Google Scholar 

  • Call J, Brauer J, Kaminski J, Tomasello M (2003) Domestic dogs (Canis familiaris) are sensitive to the attentional state of humans. J Comp Psychol 117(3):257–263

    Article  PubMed  Google Scholar 

  • Carmi R, Itti L (2006) Visual causes versus correlates of attentional selection in dynamic scenes. Vis Res 46(26):4333–4345

    Article  PubMed  Google Scholar 

  • Chawarska K, Klin A, Volkmar F (2003) Automatic attention cueing through eye movement in 2-year-old children with autism. Child Dev 74(4):1108–1122

    Article  PubMed  Google Scholar 

  • Deaner RO, Khera AV, Platt ML (2005) Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr Biol 15(6):543–548

    Article  PubMed  CAS  Google Scholar 

  • Deaner RO, Shepherd SV, Platt ML (2007) Familiarity accentuates gaze cuing in women but not men. Biol Lett 3:64–67

    Article  PubMed  Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24(6):581–604

    Article  PubMed  CAS  Google Scholar 

  • Fisher NI (1993) Statistical analysis of circular data. Cambridge University Press, Cambridge, p 32

  • Gilad Y, Wiebe V, Przeworski M, Lancet D, Paabo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2(1):E5

    Article  PubMed  Google Scholar 

  • Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581

    Article  Google Scholar 

  • Haude RH, Ray OS (1974) Visual observing behavior in the squirrel monkey. Anim Learn Behav 2:138–140

    Google Scholar 

  • Hesterberg T, Moore DS, Monaghan S, Clipson A, Epstein R (2005) Bootstrap methods and permutation tests, 2nd edn. W. H. Freeman, New York

    Google Scholar 

  • Itakura S (1996) An exploratory study of gaze monitoring in non-human primates. Jpn Psychol Res 38:174–180

    Article  Google Scholar 

  • Itakura S (2004) Gaze-following and joint visual attention in nonhuman animals. Jpn Psych Res 46(3):216–226

    Article  Google Scholar 

  • Jolly A (1966) Lemur social behavior and primate intelligence. Science 153:501–506

    Article  PubMed  CAS  Google Scholar 

  • Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ behavior from humans. Anim Cogn 7(4):216–223

    Article  PubMed  Google Scholar 

  • Kaminski J, Riedel J, Call J, Tomasello M (2005) Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task. Anim Behav 69:11–18

    Article  Google Scholar 

  • Kay R, Kirk E (2000) Osteological evidence for the evolution of activity pattern and visual acuity in primates. Am J Phys Anthropol 113(2):235–262

    Article  PubMed  CAS  Google Scholar 

  • Klin A, Jones W, Schultz R, Volkmar F, Cohen D (2002) Defining and quantifying the social phenotype in autism. Am J Psychiatry 159(6):895–908

    Article  PubMed  Google Scholar 

  • Land MF, Hayhoe M (2001) In what ways do eye movements contribute to everyday activities? Vis Res 41(25–26):3559–3565

    Article  PubMed  CAS  Google Scholar 

  • Langton SR, Watt RJ, Bruce II (2000) Do the eyes have it? Cues to the direction of social attention. Trends Cogn Sci 4(2):50–59

    Article  PubMed  Google Scholar 

  • Pariente G (1975) Observation ophtalmologique de zones fou´eles vraies chez Lemur catta et Hapalemur griseus, primates de Madagascar. Mammalia 39:487–497

    Article  Google Scholar 

  • Ristic J, Mottron L, Friesen CK, Iarocci G, Burack JA et al (2005) Eyes are special but not for everyone: the case of autism. Brain Res Cogn Brain Res 24(3):715–718

    Article  PubMed  Google Scholar 

  • Sackett GP (1966) Monkeys reared in isolation with pictures as visual input: evidence for an innate releasing mechanism. Science 154(755):1468–1473

    Article  PubMed  CAS  Google Scholar 

  • Sauther M, Sussman R, Gould L (1999) The socioecology of the ringtailed lemur: thirty-five years of research. Evolut Anthropol 8(4):120–132

    Article  Google Scholar 

  • Shepherd SV, Platt ML (2006) Noninvasive telemetric gaze tracking in freely moving socially housed prosimian primates. Methods 38(3):185–194

    Article  PubMed  CAS  Google Scholar 

  • Shepherd SV, Deaner RO, Platt ML (2006) Social status gates social attention in monkeys. Curr Biol 16(4):R119–R120

    Article  PubMed  CAS  Google Scholar 

  • Swettenham J, Condie S, Campbell R, Milne E, Coleman M (2003) Does the perception of moving eyes trigger reflexive visual orienting in autism? Philos Trans R Soc Lond B Biol Sci 358(1430):325–334

    Article  PubMed  Google Scholar 

  • Tomasello M, Call J, Hare B (1998) Five primate species follow the visual gaze of conspecifics. Anim Behav 55(4):1063–1069

    Article  PubMed  Google Scholar 

  • Tschudin A, Call J, Dunbar RI, Harris G, van der Elst C (2001) Comprehension of signs by dolphins (Tursiops truncatus). J Comp Psychol 115(1):100–105

    Article  PubMed  CAS  Google Scholar 

  • von Rohen JW, Castenholz A (1967) Über die Zentralisation der Retina bei Primaten. Folia Primat 5:92–147

    Article  CAS  Google Scholar 

  • Yoder AD, Yang Z (2004) Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 13(4):757–773

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Thanks to Kyndal Davis, Luke Stewart, Lauren Whitted, Dan Schmitt, Julie Ives, Stephanie Combes, Bill Hess, David Haring, Ben Hayden, and Chris Kirk. Lemur body silhouette in Fig. 5 adapted, with permission, from a photo by June Rubis. Supported by the Alfred P. Sloan Foundation and the Duke Lemur Center (DLC #1016).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen V. Shepherd.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary video (WMV 6291 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shepherd, S.V., Platt, M.L. Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta). Anim Cogn 11, 13–20 (2008). https://doi.org/10.1007/s10071-007-0083-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-007-0083-6

Keywords

Navigation