The Hand pp 55-73 | Cite as

Primates’ Propensity to Explore Objects: How Manual Actions Affect Learning in Children and Capuchin Monkeys

  • Fabrizio Taffoni
  • Eugenia Polizzi di Sorrentino
  • Gloria Sabbatini
  • Domenico Formica
  • Valentina Truppa
Chapter
Part of the Studies in Applied Philosophy, Epistemology and Rational Ethics book series (SAPERE, volume 38)

Abstract

Humans and other animals have a strong propensity to explore the environment. When human infants, as well as other primates, face the opportunity to interact with the environment by manipulating objects, they may discover and learn the contingency between one action and its outcome. Thus, manipulation, as a form of spontaneous exploration, has a great biological significance, since it allows to discover and learn the relationship between action and effect, enabling humans and other animals to plan goal-directed tasks. How do the specific characteristics of the primate’s body influence this process? With its large amount of degrees of freedom, sensors, and nervous terminations, the hand is the main interface with the external world, and it profoundly influences the primates’ interaction with the environment. How does object exploration mediated by manual actions affect the acquisition of problem-solving abilities? To try to answer this question, we experimentally compared how children and capuchin monkeys (Sapajus spp.)—nonhuman primates well known for their manual dexterity and for being curious and highly manipulative—acquire new cause–effect relations through spontaneous manual exploration of a new environment. The experiments were carried out with the mechatronic board, an innovative device specifically designed to allow interspecies comparative research. The board allowed testing whether spontaneous manipulation of objects (not instrumental to achieve any specific goal) improved subjects’ ability to solve a subsequent goal-directed task by retrieving the knowledge learned during previous exploration.

Keywords

Object manipulation Curiosity driven learning Action-outcome contingency Mechatronic board Behavioral analysis 

References

  1. Aversi-Ferreira, T. A., Maior, R. S., Carneiro-e Silva, F. O., Aversi-Ferreira, R. A., Tavares, M. C., Nishijo, H., & Tomaz, C. (2011). Comparative anatomical analyses of the forearm muscles of Cebus libidinosus (Rylands et al. 2000): Manipulatory behavior and tool use. PloS one, 6(7), e22165.Google Scholar
  2. Baillie, J. C. (2016). Why alphago is not AI, March 2016. Available at http://spectrum.ieee.org/automaton/robotics/artificial-intelligence/why-alphago-is-not-ai. Cited 20 December 2016.
  3. Bertenthal, B., & Von Hofsten, C. (1998). Eye, head and trunk control: the foundation for manual development. Neuroscience and Biobehavioral Reviews, 22(4), 515–520.CrossRefGoogle Scholar
  4. Bortoff, G. A., & Strick, P. L. (1993). Corticospinal terminations in two new-world primates: Further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. The Journal of Neuroscience, 13(12), 5105–5118.Google Scholar
  5. Byrne, G., & Suomi, S. J. (1996). Individual differences in object manipulation in a colony of tufted capuchins. Journal of Human Evolution, 31(3), 259–267.CrossRefGoogle Scholar
  6. Christel, M. I., & Fragaszy, D. (2000). Manual function in Cebus apella digital mobility, preshaping, and endurance in repetitive grasping. International Journal of Primatology, 21(4), 697–719.Google Scholar
  7. Cioni, G., & Giuseppina, S. (2013). Pediatric neurology part I: Chapter 1. In Normal psychomotor development. Elsevier Inc. Chapters, 111.Google Scholar
  8. Costello, M. B., & Fragaszy, D. M. (1988). Prehension in Cebus and Saimiri: I. grip type and hand preference. American Journal of Primatology, 15(3), 235–245.Google Scholar
  9. Cutkosky, M. R. (1989). On grasp choice, grasp models, and the design of hands for manufacturing tasks. Robotics and Automation, IEEE Transactions on, 5(3), 269–279.Google Scholar
  10. Fallang, B., Saugstad, O. D., & Hadders-Algra, M. (2000). Goal directed reaching and postural control in supine position in healthy infants. Behavioural Brain Research, 115(1), 9–18.Google Scholar
  11. Focaroli, V., Taffoni, F., & Iverson, J. M. (2015). Motor planning ability in typically developing children and children with autism spectrum disorder. Psicologia Clinica dello Sviluppo, 19(1), 3–26.Google Scholar
  12. Fragaszy, D. M., & Adams-Curtis, L. E. (1991). Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 105(4), 387.Google Scholar
  13. Fragaszy, D. M., & Boinski, S. (1995). Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). Journal of Comparative Psychology, 109(4), 339.Google Scholar
  14. Fragaszy, D. M., & Crast, J. (2016). Functions of the hand in Primates. In The evolution of the primate hand: Anatomical, developmental, functional, and paleontological evidence (pp. 313–344). New York: Springer.Google Scholar
  15. Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.Google Scholar
  16. Iverson, J. M. (2010). Developing language in a developing body: The relationship between motor development and language development. Journal of Child Language, 37(02), 229–261.Google Scholar
  17. Kapandji, I. A. (1987). The physiology of the joints: Lower limb (vol. 2). Elsevier Health Sciences.Google Scholar
  18. Kaplan, F., & Pierre-Yves, O. (2007). In search of the neural circuits of intrinsic motivation. Frontiers in Neuroscience, 1(1), 225–242.CrossRefGoogle Scholar
  19. Lynch Alfaro, J. W., Boubli, J. P., Olson, L. E., Di Fiore, A., Wilson, B., Gutiérrez-Espeleta, G. A., et al. (2012a). Explosive pleistocene range expansion leads to widespread amazonian sympatry between robust and gracile capuchin monkeys. Journal of Biogeography, 39(2), 272–288.Google Scholar
  20. Lynch Alfaro, J. W., Silva, J. D. S. E., & Rylands, A. B. (2012b). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74(4), 273–286.Google Scholar
  21. Napier, J. R. (1956). The prehensile movements of the human hand. Bone & Joint Journal, 38(4), 902–913.Google Scholar
  22. O’Regan, J. K., & Noë, A. (2001). A sensorimotor account of vision and visual consciousness. Behavioral and Brain Sciences, 24(05), 939–973.Google Scholar
  23. Out, L., van Soest, A. J., Savelsbergh, G. J., & Hopkins, B. (1998). The effect of posture on early reaching movements. Journal of Motor Behavior, 30(3), 260–272.Google Scholar
  24. Padberg, J., Franca, J. G., Cooke, D. F., Soares, J. G., Rosa, M. G., Fiorani, M., et al. (2007). Parallel evolution of cortical areas involved in skilled hand use. The Journal of Neuroscience, 27(38), 10106–10115.Google Scholar
  25. Panger, M. A. (1998). Object-use in free-ranging white-faced capuchins (Cebus capucinus) in costa rica. American Journal of Physical Anthropology, 106(3), 311–321.Google Scholar
  26. Perry, S., & Manson, J. H. (2008). Manipulative monkeys. Harvard University Press.Google Scholar
  27. Polizzi di Sorrentino, E., Sabbatini, G., Truppa, V., Bordonali, A., Taffoni, F., Formica, D., et al. (2014). Exploration and learning in capuchin monkeys (Sapajus spp.): the role of action–outcome contingencies. Animal Cognition, 17(5), 1081–1088.Google Scholar
  28. Preuschoft, H., & Chivers, D. J. (2012). Hands of primates. Berlin: Springer.Google Scholar
  29. Rochat, P., & Goubet, N. (1995). Development of sitting and reaching in 5-to 6-month-old infants. Infant Behavior and Development, 18(1), 53–68.CrossRefGoogle Scholar
  30. Sabbatini, G., Meglio, G., & Truppa, V. (2016). Motor planning in different grasping tasks by capuchin monkeys (Sapajus spp.). Behavioural Brain Research, 312, 201–211.CrossRefGoogle Scholar
  31. Spencer, J. P., Vereijken, B., Diedrich, F. J., & Thelen, E. (2000). Posture and the emergence of manual skills. Developmental Science, 3(2), 216–233.Google Scholar
  32. Spinozzi, G., Castorina, M. G., & Truppa, V. (1998). Hand preferences in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 112(2), 183.Google Scholar
  33. Spinozzi, G., Laganà, T., & Truppa, V. (2007). Hand use by tufted capuchins (Cebus apella) to extract a small food item from a tube: Digit movements, hand preference, and performance. American Journal of Primatology, 69(3), 336–352.CrossRefGoogle Scholar
  34. Spinozzi, G., Truppa, V., & Laganà, T. (2004). Grasping behavior in tufted capuchin monkeys (Cebus apella): Grip types and manual laterality for picking up a small food item. American Journal of Physical Anthropology, 125(1), 30–41.CrossRefGoogle Scholar
  35. Taffoni, F., Formica, D., Schiavone, G., Scorcia, M., Tomassetti, A., Polizzi di Sorrentino, E., et al. (2013). The “mechatronic board”: A tool to study intrinsic motivations in humans, monkeys, and humanoid robots. In Intrinsically motivated learning in natural and artificial systems (pp. 411–432). Berlin: Springer.Google Scholar
  36. Taffoni, F., Formica, D., Zompanti, A., Mirolli, M., Balsassarre, G., Keller, F., & Guglielmelli, E. (2012a). A mechatronic platform for behavioral studies on infants. In 2012 4th IEEE RAS & EMBS International Conference on Biomedical Robotics and Biomechatronics (BioRob) (pp. 1874–1878). IEEE.Google Scholar
  37. Taffoni, F., Tamilia, E., Focaroli, V., Formica, D., Ricci, L., Di Pino, G., et al. (2014). Development of goal-directed action selection guided by intrinsic motivations: an experiment with children. Experimental Brain Research, 232(7), 2167–2177.Google Scholar
  38. Taffoni, F., Vespignani, M., Formica, D., Cavallo, G., Polizzi di Sorrentino, E., Sabbatini, G., et al. (2012b). A mechatronic platform for behavioral analysis on nonhuman primates. Journal of Integrative Neuroscience, 11(01), 87–101.Google Scholar
  39. Terborgh, J. (1983). Five New World primates: A study in comparative ecology. Princeton University Press.Google Scholar
  40. Truppa, V., Spinozzi, G., Laganà, T., Mortari, E. P., & Sabbatini, G. (2016). Versatile grasping ability in power-grip actions by tufted capuchin monkeys (Sapajus spp.). American Journal of Physical Anthropology, 159(1), 63–72.Google Scholar
  41. Visalberghi, E. (1988). Responsiveness to objects in two social groups of tufted capuchin monkeys (Cebus apella). American Journal of Primatology, 15(4), 349–360.CrossRefGoogle Scholar
  42. Visalberghi, E., Cavallero, S., Fragaszy, D. M., Izar, P., Aguiar, R. M., & Truppa, V. (2015a). Making use of capuchins’ behavioral propensities to obtain hair samples for DNA analyses. Neotropical Primates, 22, 89–93.Google Scholar
  43. Visalberghi, E., & Fragaszy, D. (2006). What is challenging about tool use? the capuchin’s perspective. In E. A. Wasserman, T. R. Zentall (Eds.), Comparative cognition: Experimental explorations of animal intelligence (pp. 529–552).Google Scholar
  44. Visalberghi, E., Sirianni, G., Fragaszy, D., & Boesch, C. (2015b). Percussive tool use by Taï western chimpanzees and fazenda Boa Vista bearded capuchin monkeys: A comparison. Philosophical Transactions R Society B, 370(1682), 20140351.CrossRefGoogle Scholar
  45. Zander, S. L., & Judge, P. G. (2015). Brown capuchin monkeys (Sapajus apella) plan their movements on a grasping task. Journal of Comparative Psychology, 129(2), 181.Google Scholar
  46. Zander, S. L., Weiss, D. J., & Judge, P. G. (2013). The interface between morphology and action planning: A comparison of two species of New World monkeys. Animal Behaviour, 86(6), 1251–1258.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Fabrizio Taffoni
    • 1
  • Eugenia Polizzi di Sorrentino
    • 2
  • Gloria Sabbatini
    • 2
  • Domenico Formica
    • 1
  • Valentina Truppa
    • 2
  1. 1.Unit of Biomedical Robotics and Biomicrosystems, Department of EngineeringUniversità Campus Bio-Medico di RomaRomeItaly
  2. 2.Unit of Cognitive Primatology and Primate CenterISTC-CNRRomeItaly

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