Abstract
There is no research about age difference in the process of sequential learning in non-human primates. Is there any difference between young and adults in sequential learning process? Six chimpanzees (Pan troglodytes), 3 young and 3 adults, learned the Arabic numeral sequence 1 to 9 by touching the numerals on a touch-screen monitor in ascending order. Initially, the sequence always started with the numeral 1, i.e. ‘start-fixed task’. Training began with the sequence 1–2, 1–2–3, and continued sequentially up to 1–2–3–4–5–6–7–8–9. Later, the subjects were introduced to sequences that started with a random numeral, but always ended with 9, i.e. ‘end-fixed task’. Performance in the end-fixed task was worse relative to the familiar start-fixed task. After training with various sequences of adjacent numerals, the subjects were given a transfer test for the non-adjacent numerals. The results suggested that all chimpanzees indeed mastered sequential ordering, and although there was no fundamental difference in the acquisition process between the two age groups, there was a significant age difference in memory capacity. Based on their knowledge of sequential ordering, the subjects were then asked to perform a masking task in which once a subject touched the lowest numeral, the other numeral(s) turned to white squares. Performance of the masking task by young chimpanzees was better than that of adults in accuracy and degree of difficulty (number of numerals). Taken together, these data clearly demonstrate a similarity among subjects in the way chimpanzees acquire knowledge of sequential order regardless of age differences in sequential learning. Moreover, they reveal that once knowledge of sequential order is established, it can be a good index used to evaluate memory capacity in young and adult chimpanzees.
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References
Beran MJ, Pate JL, Washburn DA, Rumbaugh DM (2004) Sequential responding and planning in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). J Exp Psychol Anim Behav Proc 30:203–212
Biro D, Matsuzawa T (1999) Numerical ordering in a chimpanzee (Pan troglodytes): planning, executing and monitoring. J Comp Psychol 113:178–185
Biro D, Matsuzawa T (2001) Use of numerical symbols by the chimpanzee (Pan troglodytes): cardinals, ordinals, and the introduction of zero. Anim Cogn 4:193–199
Boysen ST, Berntson GG, Shreyer TA, Quigley KS (1993) Processing of ordinality and transitivity by chimpanzees (Pan troglodytes). J Comp Psychol 107:208–215
Chen S, Swartz KB, Terrace HS (1997) Knowledge of the ordinal position of list items in rhesus monkeys. Psychol Sci 8:80–86
Conway CM, Christiansen MH (2001) Sequential learning in non-human primates. Trends Cognit Sci 5:539–546
D’Amato MR, Colombo M (1988) Representation of serial order in monkeys (Cebus apella). J Exp Psychol Anim Behav Proc 14:131–139
Fisher AV, Sloutsky VM (2005) When induction meets memory: evidence for a gradual transition from similarity-based to category-based induction. Child Dev 76:583–597
Hayes BK, Heit E (2004) Why learning and development can lead to poorer recognition memory. Trends Cognit Sci 8:337–339
Inoue S, Matsuzawa T (2007) Working memory of numerals in chimpanzees. Curr Biol 17:1004–1005
Kawai N, Matsuzawa T (2000) Numeric memory span in a chimpanzee. Nature 403:39–40
Matsuzawa T (1985) Use of numbers by a chimpanzee. Nature 315:57–59
Matsuzawa T (2003) The Ai project: historical and ecological contexts. Anim Cogn 6:199–211
Matsuzawa T (2009a) Chimpanzee mind: looking for the evolutionary roots of the human mind. Anim Cogn. doi:10.1007/s10071-009-0277-1
Matsuzawa T (2009b) Symbolic representation of number in chimpanzees. Curr Opin Neurobiol 19:92–98
Matsuzawa T, Tomonaga M, Tanaka M (eds) (2006) Cognitive development in chimpanzees. Springer, Tokyo
Merritt D, MacLean EL, Jaffe S, Brannon EM (2007) A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta). J Comp Psychol 121:363–371
Murofushi K (1997) Numerical matching behavior by a chimpanzee (Pan troglodytes): subitizing and analogue magnitude estimation. Jpn Psychol Res 39:140–153
Ohshiba N (1997) Memorization of serial items by Japanese monkeys, a chimpanzee, and humans. Jpn Psychol Res 39:236–252
Sloutsky VM, Fisher AV (2004) When development and learning decrease memory: evidence against category-based induction in children. Psychol Sci 15:553–558
Swartz KB, Chen S, Terrace HS (1991) Serial learning by rhesus monkeys: I. Acquisition and retention of multiple four-item lists. J Exp Psychol Anim Behav Proc 17:396–410
Swartz KB, Chen S, Terrace HS (2000) Serial learning by rhesus monkeys: II. Learning four-item lists by trial and error. J Exp Psychol Anim Behav Proc 26:274–285
Terrace HS (1993) The phylogeny and ontogeny of serial memory: List learning by pigeons and monkeys. Psychol Sci 4:162–169
Terrace HS (2005) The simultaneous chain: a new approach to serial learning. Trends Cognit Sci 9:202–210
Terrace HS, Son LK, Brannon EM (2003) Serial expertise of rhesus macaques. Psychol Sci 14:66–73
Tomonaga M (2008) Relative numerosity discrimination by chimpanzees (Pan troglodytes): evidence for approximate numerical representations. Anim Cogn 11:43–57
Tomonaga M, Matsuzawa T (2000) Sequential responding to arabic numerals with wild cards by the chimpanzee (Pan troglodytes). Anim Cogn 3:1–11
Tomonaga M, Matsuzawa T (2002) Enumeration of briefly presented items by the chimpanzee (Pan troglodytes) and humans (Homo sapiens). Anim Learn Behav 30:143–157
Treichler FR, Raghanti MA (2009) Serial list combination by monkeys (Macaca mulatta): test cues and linking. Anim Cogn. doi:10.1007/s10071-009-0251-y
Treichler FR, Van Tilburg D (1999) Training requirements and retention characteristics of serial list organization by macaque monkeys. Anim Cogn 2:235–244
Treichler FR, Van Tilburg D (2002) Premise-pair training for valid tests of serial list organization in macaques. Anim Cogn 5:97–105
Treichler FR, Raghanti MA, Van Tilburg DN (2003) Linking of serially ordered lists by macaque monkeys (Macaca mulatta): list position influences. J Exp Psychol Anim Behav Proc 29:211–221
Washburn DA, Rumbaugh DM (1991) Ordinal judgments of numerical symbols by macaques (Macaca mulatta). Psychol Sci 2:190–193
Acknowledgments
This study was supported by grants MEXT16002001 and 20002001, JSPS-GCOE (A06, Biodiversity), and JSPS-HOPE to TM. This is a part of PhD thesis of SI. Thanks are due to Sumiharu Nagumo for his help with computer programming, Masaki Tomonaga, Masayuki Tanaka, Misato Hayashi, Dora Biro, Etsuko Nogami and Tomoko Takashima for their support, Armand Jacobs for his advice on statistical analyses, Christopher Martin for his English revision, and Alexander D. Hernandez for his English revision and great advice and help to the manuscript. Thanks are also due to the veterinary staffs and caregivers of the KUPRI chimpanzees.
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This contribution is part of the Supplement Issue “The Chimpanzee Mind” (Matsuzawa 2009).
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Inoue, S., Matsuzawa, T. Acquisition and memory of sequence order in young and adult chimpanzees (Pan troglodytes). Anim Cogn 12 (Suppl 1), 59–69 (2009). https://doi.org/10.1007/s10071-009-0274-4
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DOI: https://doi.org/10.1007/s10071-009-0274-4