Abstract
The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton in Proc Natl Acad Sci USA 98:5359–5362, 2001; Smith et al. in Behav Brain Sci 26:317–374, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.
Similar content being viewed by others
References
Basile BM, Hampton RR, Suomi S, Murray EA (2009) An assessment of memory awareness in tufted capuchin monkeys (Cebus apella). Anim Cogn 12(1):169–180. doi:10.1007/s10071-008-0180-1
Beran MJ, Smith JD, Redford JS, Washburn DA (2006) Rhesus macaques (Macaca mulatta) monitor uncertainty during numerosity judgments. J Exp Psychol Anim Behav Process 32(2):111–119. doi:10.1037/0097-7403.32.2.111
Beran MJ, Smith JD, Coutinho MVC, Couchman JJ, Boomer J (2009) The psychological organization of “uncertainty” responses and “middle” responses: a dissociation in capuchin monkeys (Cebus apella). J Exp Psychol Anim Behav Process 35(3):371–381. doi:10.1037/a0014626
Call J (2010) Do apes know that they could be wrong? Anim Cogn 13(5):689–700. doi:10.1007/s10071-010-0317-x
Call J, Carpenter M (2001) Do apes and children know what they have seen? Anim Cogn 4:207–220
Carruthers P (2008) Meta-cognition in animals: a skeptical look. Mind Lang 23(1):58–89
Clark RE, Manns JR, Squire LR (2002) Classical conditioning, awareness, and brain systems. Trends Cogn Sci 6(12):524–531
Couchman JJ, Coutinho MVC, Beran MJ, Smith JD (2010) Beyond stimulus cues and reinforcement signals a new approach to animal metacognition. J Comp Psychol 124(4):356–368. doi:10.1037/a0020129
Crystal JD, Foote AL (2009) Metacognition in animals. Comp Cogn Behav Rev 4:1–16
Flavell JH (1979) Meta-cognition and cognitive monitoring-new area of cognitive-developmental inquiry. Am Psychol 34(10):906–911
Foote AL, Crystal JD (2007) Metacognition in the rat. Curr Biol 17(6):551–555
Fujita K (2009) Memory awareness in tufted capuchin monkeys (Cebus apella). Anim Cogn 12(4):575–585. doi:10.1007/s10071-009-0217-0
Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER et al (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316(5822):222–234. doi:10.1126/science.1139247
Hampton RR (2001) Rhesus monkeys know when they remember. Proc Natl Acad Sci USA 98:5359–5362
Hampton RR (2009) Multiple demonstrations of metacognition in nonhumans: converging evidence or multiple mechanisms? Available from: http://psyc.queensu.ca/ccbr/index.html
Hampton RR, Zivin A, Murray EA (2004) Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting. Anim Cogn 7:239–254
Inman A, Shettleworth SJ (1999) Detecting memory awareness in nonverbal subjects: a test with pigeons. J Exp Psychol Anim Behav Process 25(3):389–395
Jozefowiez K, Staddon JER, Cerutti DT (2009) Metacognition in animals: how do we know that they know? Available from: http://psyc.queensu.ca/ccbr/index.html
Keppel G, Wickens TD (2004) Design and analysis: a researchers handbook, 4th edn. Pearson, Upper Saddle River
Kornell N, Son LK, Terrace HS (2007) Transfer of metacognitive skills and hint seeking in monkeys. Psychol Sci 18(1):64–71
Metcalfe J (2008) Evolution of metacognition. In: Bjork JDRA (ed) Handbook of memory awareness and memory. Psychology Press, New York, pp 29–46
Nakamura N, Watanabe S, Betsuyaku T, Fujita K (2011) Do birds (pigeons and bantams) know how confident they are of their perceptual decisions? Anim Cogn 14(1):83–93. doi:10.1007/s10071-010-0345-6
Nelson TO (1996) Consciousness and metacognition. Am Psychol 51(2):102–116
Roberts WA (1972) Short-term memory in pigeons-effects of repetition and spacing. J Exp Psychol Gen 94(1):74
Roberts WA, Feeney MC, McMillan N, MacPherson K, Musolino E, Petter M (2009) Do pigeons (Columba livia) study for a test? J Exp Psychol Anim Behav Process 35(2):129–142. doi:10.1037/a0013722
Sands SF, Wright AA (1980) Serial probe recognition performance by performance by a rhesus monkey and a human with 10- and 20-item lists. J Exp Psychol Anim Behav Process 6(4):386–396
Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New York
Shields WE, Smith JD, Washburn DA (1997) Uncertain responses by humans and rhesus monkeys (Macaca mulatta) in a psychophysical same-different task. J Exp Psychol Gen 126(2):147–164
Smith JD, Washburn DA (2005) Uncertainty monitoring and metacognition by animals. Curr Dir Psychol Sci 14(1):19–24
Smith JD, Schull J, Strote J, McGee K, Egnor R, Erb L (1995) The uncertain response in the bottlenosed dolphin (Tursiops truncatus). J Exp Psychol Gen 124(4):391–408
Smith JD, Shields WE, Washburn DA (1998) Memory monitoring by animals and humans. J Exp Psychol Gen 127(3):227–250
Smith JD, Shields WE, Washburn DA (2003) The comparative psychology of uncertainty monitoring and metacognition. Behav Brain Sci 26:317–374
Smith JD, Redford JS, Beran MJ, Washburn DA (2006) Dissociating uncertainty responses and reinforcement signals in the comparative study of uncertainty monitoring. J Exp Psychol Gen 135(2):282–297
Smith JD, Beran MJ, Couchman JJ, Coutinho MVC (2008) The comparative study of metacognition: sharper paradigms, safer inferences. Psychon Bull Rev 15(4):679–691. doi:10.3758/pbr.15.4.679
Smith JD, Redford JS, Beran MJ, Washburn DA (2010) Rhesus monkeys (Macaca mulatta) adaptively monitor uncertainty while multi-tasking. Anim Cogn 13(1):93–101. doi:10.1007/s10071-009-0249-5
Sole LM, Shettleworth SJ, Bennett PJ (2003) Uncertainty in pigeons. Psychon Bull Rev 10(3):738–745
Squire LR, Zola-Morgan S (1991) The medial temporal-lobe memory system. Science 253(5026):1380–1386
Suda-King C (2008) Do orangutans (Pongo pygmaeus) know when they do not remember? Anim Cogn 11(1):21–42
Sutton JE, Shettleworth SJ (2008) Memory without awareness: pigeons do not show memory awareness in delayed matching to sample. J Exp Psychol Anim Behav Process 34(2):266–282
Acknowledgments
A version of this paper was submitted in partial fulfillment for a master’s thesis at Emory University. Joseph Manns, Stella Lourenco, and Jocelyn Bachevalier provided helpful comments on an early draft. This research was supported by the National Institute of Mental Health Grant No. R01MH082819 and the National Science Foundation Grant No. 0000017475. Additional support was provided by the Yerkes Center base grant No. RR-00165 awarded by the Animal Resources Program of the National Institutes of Health, and the Center for Behavioral Neuroscience under the STC Program of the National Science Foundation under Agreement No. IBN-9876754. These experiments comply with US law.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Templer, V.L., Hampton, R.R. Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests. Anim Cogn 15, 409–419 (2012). https://doi.org/10.1007/s10071-011-0468-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-011-0468-4