Skip to main content
Log in

Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test

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

Abstract

Self-directed behaviors (SDBs) are a commonly used behavioral indicator of arousal in nonhuman primates. Experimental manipulations, designed to increase arousal and uncertainty, have been used to elicit SDB production in primates. Beyond measuring rates of SDB production, researchers have also recorded their lateralized production by primates, thought to reflect laterality of hemispheric brain control and response to emotion. Although a handful of such studies exist, all have been conducted with chimpanzees. Expanding on this line of inquiry, we tested both chimpanzees (N = 3) and gorillas (N = 3) in a serial learning task presented on a touchscreen interface that incorporated both EASY (two-item list) and HARD (four-item list) versions of the task. Although SDB production by the apes did not differ across the two levels of task complexity, both species produced higher rates of SDB when they made an error, regardless of task difficulty. Furthermore, the apes made more SDB with the left hand—directed to the right side of their body (contralateral SDB) and left side of their body (ipsilateral SDB)—when they made an incorrect response. There was no difference in the rate of SDB produced with the right hand across correct compared to incorrect trials. The apes’ responses reflect previous reports that show humans are quicker at selecting negative emotional stimuli when using their left, compared to their right, hand (the reverse is true for positive stimuli). However, previous work has shown that chimpanzees are more likely to produce (contralateral) SDB with their right hand when aroused and so we discuss our results in relation to these findings and consider how they relate to the ‘right hemisphere’ and ‘valence’ models of emotional processing in apes.

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

Similar content being viewed by others

References

  • Alfano KM, Cimino CR (2008) Alteration of expected hemispheric asymmetries: valence and arousal effects in neuropsychological models of emotion. Brain Cogn 66(3):213–220

    Article  PubMed  Google Scholar 

  • Borod JC, Cicero BA, Obler LK, Welkowitz J, Erhan HM, Santaschi C, Grunwald IS, Agosti RM, Whalen JR (1998) Right hemisphere emotional perception: evidence across multiple channels. Neuropsychology 12(3):446–458

    Article  CAS  PubMed  Google Scholar 

  • Braccini SN, Lambeth SP, Schapiro SJ, Fitch WT (2012) Eye preferences in captive chimpanzees. Anim Cogn 15(5):971–978

    Article  PubMed  Google Scholar 

  • Clay AW, Perdue BM, Gaalema DE, Dolins FL, Bloomsmith MA (2011) The use of technology to enhance zoological parks. Zoo Biol 30(5):487–497

    Article  PubMed  Google Scholar 

  • Davidson RJ (1992a) Anterior cerebral asymmetry and the nature of emotion. Brain Cogn 20(1):125–151

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Gluck JP, Sackett GP (1976) Extinction deficits in socially isolated rhesus monkeys (Macaca mulatta). Dev Psychol 12:173–174

    Article  Google Scholar 

  • Gordon DJ, Rogers LJ (2015) Cognitive bias, hand preference and welfare of common marmosets. Behav Brain Res 287:100–108

    Article  PubMed  Google Scholar 

  • Harding EJ, Paul ES, Mendl M (2004) Cognitive bias and affective state. Nature 427:312

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hook-Costigan M, Rogers LJ (1998) Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychology 36:1265–1273

    Article  CAS  Google Scholar 

  • Hopkins WD (1995) Hand preferences from a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. J Comp Psychol 109(3):291–297

    Article  CAS  PubMed  Google Scholar 

  • Hopkins WD, Russell JL, Freeman H, Reynolds EAM, Griffis C, Leavens DA (2006) Lateralized scratching in chimpanzees (Pan troglodytes): evidence of a functional asymmetry during arousal. Emotion 6(4):553–559

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopper LM, Morgan DB, Ross SR (2014) The next direction for primatology? A commentary on Setchell (2013). Int J Primatol 35(2):341–348

    Article  Google Scholar 

  • Itakura S (1993) Emotional behaviour during the learning of a contingency task in a chimpanzee. Percept Motor Skills 76(2):563–566

    Article  CAS  PubMed  Google Scholar 

  • Judge PG, Evans DW, Schroepfer KK, Gross AC (2011) Perseveration on a reversal-learning task correlates with rates of self-directed behavior in nonhuman primates. Behav Brain Res 222:57–65

    Article  PubMed  Google Scholar 

  • Kawai N, Matsuzawa T (2000) Cognition: numerical memory span in a chimpanzee. Nature 403(6765):39–40

    Article  CAS  PubMed  Google Scholar 

  • Killgore WD, Yurgelun-Todd DA (2004) Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 21(4):1215–1223

    Article  PubMed  Google Scholar 

  • Leavens DA, Aureli F, Hopkins WD, Hyatt CW (2001) Effects of cognitive challenge on self-directed behaviors by chimpanzees (Pan troglodytes). Am J Primatol 55(1):1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leavens DA, Aureli F, Hopkins WD (2004) Behavioral evidence for the cutaneous expression of emotion in a chimpanzee (Pan troglodytes). Behaviour 141(8):979–997

    Article  Google Scholar 

  • Leliveld LMC, Langbein J, Puppe B (2013) The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Appl Anim Behav Sci 145(1–2):1–14

    Article  Google Scholar 

  • Maestripieri D, Schino G, Aureli F, Troisi A (1992) A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 44:967–979

    Article  Google Scholar 

  • Nakayama K (2004) Observing conspecifics scratching induces a contagion of scratching in Japanese monkeys (Macaca fuscata). J Comp Psychol 118(1):20–24

    Article  PubMed  Google Scholar 

  • Price A, Boeving ER, Shender MA, Ross SR (2015) Understanding the effectiveness of demonstration programs. J Mus Educ 40(1):46–54

    Article  Google Scholar 

  • Quaresmini C, Forrester GS, Speizio C, Vallortigara G (2014) Social environment elicits lateralized behaviours in gorillas and chimpanzees. J Comp Psychol 128(3):276–284

    Article  PubMed  Google Scholar 

  • Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73(2):236–253

    Article  CAS  PubMed  Google Scholar 

  • Root JC, Wong PS, Kinsbourne M (2006) Left hemisphere specialization for response to positive emotional expressions: a divided output methodology. Emotion 6(3):473–483

    Article  PubMed  Google Scholar 

  • Ross SR (2009) Sequential list-learning by an adolescent lowland gorilla (Gorilla gorilla gorilla) using an infrared touchframe apparatus. Interact Stud 10(2):115–129

    Article  Google Scholar 

  • Schino G, Troisi A, Peretta G, Monaco V (1991) Measuring anxiety in nonhuman primates: effect of lorazepam on macaque scratching. Pharm Biochem Behav 38:889–891

    Article  CAS  Google Scholar 

  • Schwartz GE, Davidson RJ, Maer F (1975) Right hemisphere lateralization for emotion in the human brain: interactions with cognition. Science 190(4211):286–288

    Article  CAS  PubMed  Google Scholar 

  • Terrace HS (2005) The simultaneous chain: a new approach to serial learning. Trends Cogn Sci 9(4):202–210

    Article  PubMed  Google Scholar 

  • Tronick EZ (1989) Emotions and emotion communication in infants. Am Psychol 44(2):112–119

    Article  CAS  PubMed  Google Scholar 

  • van Lawick-Goodall J (1972) A preliminary report on expressive movements and communication in the Gombe stream chimpanzees. In: Dolhinow P (ed) Primate patterns. Holt, Rinehart and Winston, New York, pp 25–84

    Google Scholar 

  • Wallez C, Vauclair J (2011) Right hemisphere dominance for emotion processing in baboons. Brain Cogn 75(2):164–169

    Article  PubMed  Google Scholar 

  • Whitehouse J, Waller BM, Chanvin M, Wallace EK, Schel AM, Peirce K, Mitchell H, Macri A, Slocombe K (2014) Evaluation of public engagement activities to promote science in a zoo environment. PLoS ONE 9(11):e113395

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamanashi Y, Matsuzawa T (2010) Emotional consequences when chimpanzees (Pan troglodytes) face challenges: individual differences in self-directed behaviours during cognitive tasks. Anim Welf 19:25–30

    CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to William Hopkins and an anonymous reviewer who provided helpful feedback on an earlier draft of this manuscript. We would like to express our gratitude to the David Bohnett Foundation for their financial support of this research and to the Animal Care staff members at the Regenstein Center for African Apes, Lincoln Park Zoo, for their ongoing dedication and critical support of this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen R. Ross.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wagner, K.E., Hopper, L.M. & Ross, S.R. Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test. Anim Cogn 19, 343–350 (2016). https://doi.org/10.1007/s10071-015-0937-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-015-0937-2

Keywords

Navigation