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Social Relationships in Nonhuman Primates: Potential Models of Pervasive Disorders

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Part of the book series: Neuromethods ((NM,volume 100))

Abstract

The diagnosis of autism in humans is currently based on behavioral criteria, including impairments in social behavior and communicative skills, and the presence of stereotypic behavior. In this chapter, we draw on behavioral parallels between humans and nonhuman primates, and propose the use of chimpanzees as a noninvasive model for understanding the development of behavioral traits associated with autism. We first examined the literature on behavioral deficits in apes. Then, using the Hominoid Personality Questionnaire (HPQ), we developed an Autism Scale for chimpanzees. This was accomplished by first asking six raters with experience of autism to rate each trait from the HPQ (a total of 54 items) on how strongly it was associated with autism. Each trait was weighted based on its mean rating, and the sum of scores on these traits, for 176 chimpanzees, was then used to produce an overall Autism Score for each chimpanzee. On this scale, we found that males scored significantly higher than females (b = 0.33, df = 1, 174, p < 0.05). We also examined mean trait differences for individuals in the upper and lower quartiles of the Autism Scale. We found low concurrence between the trait loadings and our predictions—which built on previous findings of stereotypic behavior induced by the environment; this suggests that the traits exhibited may be associated with neurodevelopmental deficits, and not simply a result of environmental trauma. We discuss the application of the Autism Scale to understanding neurodevelopmental disorders in nonhuman primates at the behavioral level.

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Notes

  1. 1.

    At the time of writing, the DSM-IV-TR (2000) defined autism using the triad of impairments. Since then, this definition has been reduced to a dyad of impairments (DSM-5, 2013); however, the behaviors within these categories remain similar to those addressed in this chapter.

References

  1. Watson KK, Platt ML (2012) Of mice and monkeys: using non-human primate models to bridge mouse- and human-based investigations of autism spectrum disorders. J Neurodev Disord 4(21):1–10

    Google Scholar 

  2. Panksepp J (1982) Toward a general psychobiological theory of emotions. Behav Brain Sci 5:407–467

    Article  Google Scholar 

  3. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    Article  CAS  PubMed  Google Scholar 

  4. Panksepp J (2011) The basic emotional circuits of mammalian brains: do animals have affective lives? Neurosci Biobehav Rev 35(9):1791–1804

    Article  PubMed  Google Scholar 

  5. Baron-Cohen S, Belmonte MK (2005) Autism: a window onto the development of the social and the analytic brain. Annu Rev Neurosci 28:109–126

    Article  CAS  PubMed  Google Scholar 

  6. American Psychiatric Association (2000) The diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Publishing, Washington, DC

    Google Scholar 

  7. Grandin T, Johnson C (2005) Animals in translation. Bloomsbury Publishing Plc, London

    Google Scholar 

  8. Baron-Cohen S et al (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31(1):5–17

    Article  CAS  PubMed  Google Scholar 

  9. Baron-Cohen S (2000) Theory of mind and autism: a review. Int Rev Res Mental Retard 23:169–184

    Article  Google Scholar 

  10. Baron-Cohen S, Leslie AM, Frith U (1985) Does the autistic child have a “theory of mind”? Cognition 21:37

    Article  CAS  PubMed  Google Scholar 

  11. Bugnyar T, Kotrschal K (2004) Leading a conspecific away from food in ravens (Corvus corax)? Anim Cogn 7(2):69–76

    Article  PubMed  Google Scholar 

  12. Schmelz M, Call J, Tomasello M (2011) Chimpanzees know that others make inferences. Proc Natl Acad Sci U S A 108(7):3077–3079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Crockford C et al (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22(2):142–146

    Article  CAS  PubMed  Google Scholar 

  14. Viranyi Z et al (2006) A nonverbal test of knowledge attribution: a comparative study on dogs and children. Anim Cogn 9(1):13–26

    Article  PubMed  Google Scholar 

  15. Call J, Tomasello M (2008) Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12(5):187–192

    Article  PubMed  Google Scholar 

  16. Pardo CA, Eberhart CG (2007) The neurobiology of autism. Brain Pathol 17(4):434–447

    Article  CAS  PubMed  Google Scholar 

  17. Gibson KR (2002) Evolution of human intelligence: the roles of brain size and mental construction. Brain Behav Evol 59:10–20

    Article  PubMed  Google Scholar 

  18. Dapretto M et al (2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9(1):28–30

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Southgate V, Hamilton AF (2008) Unbroken mirrors: challenging a theory of autism. Trends Cogn Sci 12(6):225–229

    Article  PubMed  Google Scholar 

  20. Ferrari PF et al (2003) Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17(8):1703–1714

    Article  PubMed  Google Scholar 

  21. Silverman JL et al (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11(7):490–502

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. King JE, Figueredo AJ (1997) The five-factor model plus dominance in chimpanzee personality. J Res Pers 31:257–271

    Article  Google Scholar 

  23. Tomonaga M et al (2004) Development of social cognition in infant chimpanzees (Pan troglodytes): face recognition, smiling, gaze, and the lack of triadic interactions. Jpn Psychol Res 46(3):227–235

    Article  Google Scholar 

  24. Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23(4):707–740

    Article  Google Scholar 

  25. Smuts B et al (1987) Primate societies. University of Chicago Press, Chicago, IL

    Google Scholar 

  26. van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87(1/2):120–144

    Article  Google Scholar 

  27. Boinski S et al (2002) An expanded test of the ecological model of primate social evolution: competitive regimes and female bonding in three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 139(2/3):227–261

    Article  Google Scholar 

  28. Mitchell CL, Boinski S, van Schaik CP (1991) Competitive regimes and female bonding in two species of squirrel monkeys (Saimiri oerstedi and S. sciureus). Behav Ecol Sociobiol 28:55–60

    Article  Google Scholar 

  29. Sussman RW, Garber PA (2011) Cooperation, collective action, and competition in primate social interactions. In: Campbell CJ et al (eds) Primates in perspective, 2nd edn. Oxford University Press, New York, NY, pp 587–599

    Google Scholar 

  30. Chapman CA, Lefebvre L (1990) Manipulating foraging group size: spider monkey food calls at fruiting trees. Anim Behav 39:891–896

    Article  Google Scholar 

  31. Murray CM, Eberly LE, Pusey AE (2006) Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behav Ecol 17(6):1020–1028

    Article  Google Scholar 

  32. Silk JB, Seyfarth RM, Cheney DL (1999) The structure of social relationships among female savanna baboons in Moremi Reserve, Botswana. Behaviour 136(6):679–703

    Article  Google Scholar 

  33. Seyfarth RM, Cheney DL (2005) The structure of social knowledge in monkeys. In: Waal FD, Tyac P (eds) Animal social complexity: intelligence, culture and individualized societies. Howard University Press, Cambridge, MA, pp 207–229

    Google Scholar 

  34. Cheney DL, Seyfarth RM, Silk JB (1995) The responses of female baboons (Papio cynocephalus ursinus) to anomalous social interactions: evidence for causal reasoning? J Comp Psychol 109(2):134–141

    Article  CAS  PubMed  Google Scholar 

  35. Engh AL et al (2006) Who, me? Can baboons infer the target of vocalizations? Anim Behav 71(2):381–387

    Article  Google Scholar 

  36. Gomez JC (1998) Do concepts of intersubjectivity apply to non-human primates? In: Bråten S (ed) Intersubjective communication and emotion in early ontogeny. Cambridge University Press, Cambridge, pp 245–259

    Google Scholar 

  37. Trevarthen C (1979) Communication and cooperation in early infancy: a description of primary intersubjectivity. In: Bullowa M (ed) Before speech: the beginning of interpersonal communication. Cambridge University Press, Cambridge, pp 321–348

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  39. Wimmer H, Perner J (1983) Beliefs about beliefs: representation and constraining function of wrong beliefs in young children’s understanding of deception. Cognition 13:103–128

    Article  CAS  PubMed  Google Scholar 

  40. Mitani JC, McGrew WC, Wrangham R (2006) Toshisada Nishida’s contributions to primatology. Primates 47(1):2–5

    Article  PubMed  Google Scholar 

  41. Bard KA et al (2011) Neurobehavioral integrity of chimpanzee newborns: comparisons across groups and across species reveal gene-environment interaction effects. Infant Child Dev 20(1):47–93

    Article  PubMed Central  PubMed  Google Scholar 

  42. Whiten A (2011) The scope of culture in chimpanzees, humans and ancestral apes. Philos Trans R Soc Lond B Biol Sci 366(1567):997–1007

    Article  PubMed Central  PubMed  Google Scholar 

  43. Goodall J (2000) In the shadow of man. Mariner Books, New York, NY

    Google Scholar 

  44. Parr LA et al (2007) Classifying chimpanzee facial expressions using muscle action. Emotion 7(1):172–181

    Article  PubMed Central  PubMed  Google Scholar 

  45. Slocombe K, Zuberbühler K (2010) Vocal communication in chimpanzees. In: Lonsdorf EV, Ross SR, Matsuzawa T (eds) The mind of the chimpanzee: ecological and experimental perspectives. University of Chicago Press, Chicago, IL, pp 192–207

    Google Scholar 

  46. Reimers M, Schwarzenberger F, Preuschoft S (2007) Rehabilitation of research chimpanzees: stress and coping after long-term isolation. Horm Behav 51(3):428–435

    Article  PubMed  Google Scholar 

  47. van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40(1):69–86

    Article  PubMed  Google Scholar 

  48. Galdikas BM (1985) Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. Am J Primatol 8(2):87–99

    Article  Google Scholar 

  49. Miller LC, Nadler RD (1981) Mother-infant relations and infant development in captive chimpanzees and orang-utans. Int J Primatol 2(3):247–261

    Article  Google Scholar 

  50. Galdikas BMF (1995) Social and reproductive behaviour of wild adolescent female orang-utans. In: Nadler RD et al (eds) The neglected ape. Plenum Press, New York, NY, pp 163–182

    Chapter  Google Scholar 

  51. Edwards SD, Snowdon CT (1980) Social behavior of captive, group-living orang-utans. Int J Primatol 1(1):39–62

    Article  CAS  Google Scholar 

  52. Liebal K, Pika S, Tomasello M (2006) Gestural communication of orangutans (Pongo pygmaeus). Gesture 6(1):1–38

    Article  Google Scholar 

  53. Stokes EJ, Parnell RJ, Olejniczak C (2003) Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav Ecol Sociobiol 54(4):329–339

    Article  Google Scholar 

  54. Watts DP (1994) Behav Ecol Sociobiol 34(5):347–358

    Article  Google Scholar 

  55. Parnell RJ (2002) The social structure and behaviour of Western Lowland Gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo, in School of Natural Sciences legacy departments, University of Stirling. http://hdl.handle.net/1893/3432

  56. Harcourt AH, Stewart KJ (1996) Function and meaning of wild gorilla ‘Close’ calls 2. Correlations with rank and relatedness. Behaviour 133(11/12):827–845

    Article  Google Scholar 

  57. Genty E et al (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn 12(3):527–546

    Article  PubMed Central  PubMed  Google Scholar 

  58. Meder A (1989) Effects of hand-rearing on the behavioral development of infant and juvenile gorillas (Gorilla g. gorilla). Dev Psychobiol 22(4):357–376

    Article  CAS  PubMed  Google Scholar 

  59. O’Connell SM (1995) Empathy in chimpanzees: evidence for theory of mind? Primates 36(3):397–410

    Article  Google Scholar 

  60. Parr LA (2001) Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Anim Cogn 4(3–4):223–229

    Article  CAS  PubMed  Google Scholar 

  61. Anderson JR, Myowa-Yamakoshi M, Matsuzawa T (2004) Contagious yawning in chimpanzees. Proc Biol Sci 271(Suppl 6):S468–S470

    Article  PubMed Central  PubMed  Google Scholar 

  62. Herrmann E, Call J (2012) Are there geniuses among the apes? Philos Trans R Soc Lond B Biol Sci 367(1603):2753–2761

    Article  PubMed Central  PubMed  Google Scholar 

  63. Watling RL, Deitz J, White O (2001) Comparison of sensory profile scores of young children with and without autism spectrum disorders. Am J Occup Ther 55:416–423

    Article  CAS  PubMed  Google Scholar 

  64. Ridley RM, Baker HF (1982) Stereotypy in monkeys and humans. Psychol Med 12(01):61–72

    Article  CAS  PubMed  Google Scholar 

  65. Harlow HF (1958) The nature of love. Am Psychol 13:673–685

    Article  Google Scholar 

  66. Suomi SJ, Harlow HF (1972) Depressive behavior in young monkeys subjected to vertical chamber confinement. J Comp Physiol Psychol 180(1):11–18

    Article  Google Scholar 

  67. Mitchell GD et al (1966) Long-term effects of total social isolation upon behaviour of rhesus macaques. Psychol Rep 18:567–580

    Article  Google Scholar 

  68. Ruppenthal GC et al (1976) A 10-year perspective of motherless-mother monkey behavior. J Abnorm Psychol 85(4):341–349

    Article  CAS  PubMed  Google Scholar 

  69. Martin LJ et al (1991) Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions. J Neurosci 11(11):3344–3358

    CAS  PubMed  Google Scholar 

  70. Gross AN et al (2011) Cage-induced stereotypies in female ICR CD-1 mice do not correlate with recurrent perseveration. Behav Brain Res 216(2):613–620

    Article  PubMed  Google Scholar 

  71. Perry BD et al (1995) Childhood trauma, the neurobiology of adaptation, and “use-dependent” development of the brain: how “states” become “traits”. Infant Mental Health J 16(4):271–291

    Article  Google Scholar 

  72. Weiss A et al (2009) Assessing chimpanzee personality and subjective well-being in Japan. Am J Primatol 71(4):283–292

    Article  PubMed  Google Scholar 

  73. Konecna M et al (2008) Personality in free-ranging Hanuman langur (Semnopithecus entellus) males: subjective ratings and recorded behavior. J Comp Psychol 122(4):379–389

    Article  PubMed  Google Scholar 

  74. Weiss A, King JE, Perkins L (2006) Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelii). J Pers Soc Psychol 90(3):501–511

    Article  PubMed  Google Scholar 

  75. Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86(2):420–428

    Article  CAS  PubMed  Google Scholar 

  76. Yeargin-Allsopp M et al (2003) Prevalence of autism in a US metropolitan area. J Am Med Assoc 289(1):150–155

    Article  Google Scholar 

  77. Baron-Cohen S (2002) The extreme male brain theory of autism. Trends Cogn Sci 6:248–254

    Article  PubMed  Google Scholar 

  78. Schulte-Ruther M et al (2008) Gender differences in brain networks supporting empathy. Neuroimage 42(1):393–403

    Article  PubMed  Google Scholar 

  79. Tripp JK (1985) Increasing activity in captive orangutans: provision of manipulable and edible materials. Zoo Biol 4(3):225–234

    Article  Google Scholar 

  80. Wilson SF (1982) Environmental influences on the activity of captive apes. Zoo Biol 1(3):201–209

    Article  Google Scholar 

  81. van Ijzendoorn MH et al (2009) Enhancement of attachment and cognitive development of young nursery-reared chimpanzees in responsive versus standard care. Dev Psychobiol 51(2):173–185

    Article  PubMed  Google Scholar 

  82. Kalcher E et al (2008) Differential onset of infantile deprivation produces distinctive long-term effects in adult ex-laboratory chimpanzees (Pan troglodytes). Dev Psychobiol 50(8):777–788

    Article  PubMed  Google Scholar 

  83. Descovich KA et al (2011) Fostering appropriate behavior in rehabilitant orangutans (Pongo pygmaeus). Int J Primatol 32(3):616–633

    Article  Google Scholar 

  84. Davenport RK, Menzel EW (1963) Stereotyped behavior of the infant chimpanzee. Arch Gen Psychiatry 8:99–120

    Article  PubMed  Google Scholar 

  85. Nadler RD, Codner MA (1983) Maternal separation and reunion of an infant orang-utan. Primates 24(1):67–76

    Article  Google Scholar 

  86. Whilde J, Marples N (2011) The behavior of a zoo-housed infant orangutan after the death of its mother. Zoo Biol 30(2):205–211

    Article  PubMed  Google Scholar 

  87. Hoff MP et al (1994) Separation and depression in infant gorillas. Dev Psychobiol 27(7):439–452

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Vanessa A. D. Wilson .

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Wilson, V.A.D., Weiss, A. (2015). Social Relationships in Nonhuman Primates: Potential Models of Pervasive Disorders. In: Roubertoux, P. (eds) Organism Models of Autism Spectrum Disorders. Neuromethods, vol 100. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-2250-5_11

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  • DOI: https://doi.org/10.1007/978-1-4939-2250-5_11

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