Exploration and learning in capuchin monkeys (Sapajus spp.): the role of action–outcome contingencies

Animals have a strong propensity to explore the environment. Spontaneous exploration has a great biological significance since it allows animals to discover and learn the relation between specific behaviours and their consequences. The role of the contingency between action and outcome for learning has been mainly investigated in instrumental learning settings and much less in free exploration contexts. We tested 16 capuchin monkeys (Sapajus spp.) with a mechatronic platform that allowed complex modules to be manipulated and to produce different outcomes. Experimental subjects could manipulate the modules and discover the contingencies between their own specific actions and the outcomes produced (i.e., the opening and lighting of a box). By contrast, Control subjects could operate on the modules, but the outcomes experienced were those performed by their paired Experimental subjects (“yoked-control” paradigm). In the exploration phase, in which no food reward was present, Experimental subjects spent more time on the board and manipulated the modules more than Yoked subjects. Experimental subjects outperformed Yoked subjects in the following test phase, where success required recalling the effective action so to open the box, now baited with food. These findings demonstrate that the opportunity to experience action–outcome contingencies in the absence of extrinsic rewards promotes capuchins’ exploration and facilitates learning processes. Thus, this intrinsically motivated learning represents a powerful mechanism allowing the acquisition of skills and cognitive competence that the individual can later exploit for adaptive purposes.

[1]  H. Harlow,et al.  Learning motivated by a manipulation drive. , 1950, Journal of experimental psychology.

[2]  R. Butler Incentive conditions which influence visual exploration. , 1954, Journal of experimental psychology.

[3]  G. B. Kish Learning when the onset of illumination is used as reinforcing stimulus. , 1955, Journal of comparative and physiological psychology.

[4]  R. Butler Discrimination learning by rhesus monkeys to auditory incentives. , 1957, Journal of comparative and physiological psychology.

[5]  R. W. White Motivation reconsidered: the concept of competence. , 1959, Psychological review.

[6]  M. Seligman,et al.  Failure to escape traumatic shock. , 1967, Journal of experimental psychology.

[7]  R. Rescorla Probability of shock in the presence and absence of CS in fear conditioning. , 1968, Journal of comparative and physiological psychology.

[8]  Light Deprivation and Sensory Reinforced Behavior in Chicks , 1971, Perceptual and motor skills.

[9]  P. Glow,et al.  Sound and light preference behaviour in naive adult rats , 1972 .

[10]  M. Seligman,et al.  Learned helplessness in the rat: time course, immunization, and reversibility. , 1975, Journal of comparative and physiological psychology.

[11]  Peter H. Glow,et al.  Response-contingent sensory change in a causally structured environment , 1978 .

[12]  Holger Ursin,et al.  Coping and Health , 1980 .

[13]  Megan R. Gunnar,et al.  Control, warning signals, and distress in infancy. , 1980 .

[14]  M. Gunnar Contingent Stimulation: A Review of its Role in Early Development , 1980 .

[15]  A. Winefield,et al.  Active versus passive control in sensory contingent bar pressing in rats. , 1980, The Journal of general psychology.

[16]  J. Terborgh Five New World Primates , 1984 .

[17]  D. Rasmussen Five New World Primates: A Study in Comparative Ecology, John Terborgh. Princeton University Press, Princeton, New Jersey (1984), xiv, +260. Price $13.50 , 1985 .

[18]  S. Mineka,et al.  Control and early socioemotional development: Infant rhesus monkeys reared in controllable versus uncontrollable environments. , 1986 .

[19]  Elisabetta Visalberghi,et al.  Responsiveness to objects in two social groups of tufted capuchin monkeys (Cebus apella) , 1988, American journal of primatology.

[20]  D. Lindburg,et al.  Vocal behavior of captive Sichuan golden monkeys (Rhinopithecus r. roxellana) , 1988, American journal of primatology.

[21]  D. Fragaszy,et al.  Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella). , 1991, Journal of comparative psychology.

[22]  P. Kalivas,et al.  Involvement of dopamine and excitatory amino acid transmission in novelty-induced motor activity. , 1994, The Journal of pharmacology and experimental therapeutics.

[23]  Dorothy M Fragaszy,et al.  Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). , 1995, Journal of comparative psychology.

[24]  S. Suomi,et al.  Individual differences in object manipulation in a colony of tufted capuchins , 1996 .

[25]  T. Nokes,et al.  Intrinsic reinforcing properties of putatively neutral stimuli in an instrumental two-lever discrimination task , 1996 .

[26]  R. Hughes,et al.  Intrinsic exploration in animals: motives and measurement , 1997, Behavioural Processes.

[27]  J. Pearce Animal Learning and Cognition: An Introduction , 1997 .

[28]  M A Panger,et al.  Object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica. , 1998, American journal of physical anthropology.

[29]  E. Deci,et al.  Self-determination theory and the facilitation of intrinsic motivation, social development, and well-being. , 2000, The American psychologist.

[30]  E. Deci,et al.  Intrinsic and Extrinsic Motivations: Classic Definitions and New Directions. , 2000, Contemporary educational psychology.

[31]  W. Mason,et al.  Cognitive style: problem solving by rhesus macaques (Macaca mulatta) reared with living or inanimate substitute mothers. , 2000, Journal of comparative psychology.

[32]  Tx Station Stata Statistical Software: Release 7. , 2001 .

[33]  P. Dayan,et al.  Reward, Motivation, and Reinforcement Learning , 2002, Neuron.

[34]  W. K. Cullen,et al.  Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty , 2003, Nature Neuroscience.

[35]  E. Ottoni,et al.  Semifree-ranging Tufted Capuchins (Cebus apella) Spontaneously Use Tools to Crack Open Nuts , 2001, International Journal of Primatology.

[36]  Nuttapong Chentanez,et al.  Intrinsically Motivated Learning of Hierarchical Collections of Skills , 2004 .

[37]  C. Fiorillo The uncertain nature of dopamine , 2004, Molecular Psychiatry.

[38]  E. Visalberghi,et al.  The Complete Capuchin: The Biology of the Genus Cebus , 2004 .

[39]  Wolfram Schultz,et al.  Rewarding properties of visual stimuli , 2005, Experimental Brain Research.

[40]  P. Redgrave,et al.  The short-latency dopamine signal: a role in discovering novel actions? , 2006, Nature Reviews Neuroscience.

[41]  G. Baldassarre,et al.  Evolving internal reinforcers for an intrinsically motivated reinforcement-learning robot , 2007, 2007 IEEE 6th International Conference on Development and Learning.

[42]  Pierre-Yves Oudeyer,et al.  Intrinsic Motivation Systems for Autonomous Mental Development , 2007, IEEE Transactions on Evolutionary Computation.

[43]  J. Manson,et al.  Manipulative Monkeys: The Capuchins of Lomas Barbudal , 2008 .

[44]  Gloria Sabbatini,et al.  Tool choice on the basis of rigidity in capuchin monkeys , 2011, Animal Cognition.

[45]  Marta Coelho Antunes,et al.  The novel object recognition memory: neurobiology, test procedure, and its modifications , 2011, Cognitive Processing.

[46]  Kevin Gurney,et al.  A Novel Task for the Investigation of Action Acquisition , 2012, PloS one.

[47]  H. Buchanan-Smith,et al.  The psychology of control: Effects of control over supplementary light on welfare of marmosets , 2012 .

[48]  Domenico Formica,et al.  A mechatronic platform for behavioral analysis on nonhuman primates. , 2012, Journal of integrative neuroscience.

[49]  Kenneth L Chiou,et al.  Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys , 2012 .

[50]  A. Rylands,et al.  How Different Are Robust and Gracile Capuchin Monkeys? An Argument for the Use of Sapajus and Cebus , 2012, American journal of primatology.

[51]  Marco Mirolli,et al.  Phasic dopamine as a prediction error of intrinsic and extrinsic reinforcements driving both action acquisition and reward maximization: A simulated robotic study , 2013, Neural Networks.

[52]  Marco Mirolli,et al.  Intrinsically Motivated Learning in Natural and Artificial Systems , 2013 .

[53]  Marco Mirolli,et al.  Intrinsically Motivated Learning Systems: An Overview , 2013, Intrinsically Motivated Learning in Natural and Artificial Systems.

[54]  M. Heisenberg,et al.  Flies Cope with Uncontrollable Stress by Learned Helplessness , 2013, Current Biology.

[55]  C. Cunningham Tool Use in Animals. Cognition and Ecology Crickette M. Sanz Josep , 2013, Animal Behaviour.

[56]  E. Visalberghi,et al.  Wild Bearded Capuchins Process Cashew Nuts Without Contacting Caustic Compounds , 2013, American journal of primatology.

[57]  J. Call,et al.  Tool use in animals : Cognition and ecology , 2013 .

[58]  Marco Mirolli,et al.  Functions and Mechanisms of Intrinsic Motivations , 2013, Intrinsically Motivated Learning in Natural and Artificial Systems.

[59]  E. Visalberghi,et al.  Tool Use in Animals: The Etho- Cebus Project: Stone-tool use by wild capuchin monkeys , 2013 .

[60]  R. Byrne,et al.  Animal curiosity , 2013, Current Biology.

[61]  E. Guglielmelli,et al.  Development of goal-directed action selection guided by intrinsic motivations: an experiment with children , 2014, Experimental Brain Research.

[62]  Kae Nakamura,et al.  Predictive Reward Signal of Dopamine Neurons , 2015 .