Abstract
The recall of a list of items in a serial order is a basic cognitive skill1. However, it is unknown whether a list of arbitrary items is remembered by associations between sequential items2,3 or by associations between each item and its ordinal position4. Here, to study the nonverbal strategies used for such memory tasks5,6,7,8,9, we trained three macaque monkeys on a delayed sequence recall task. Thirty abstract images, divided into ten triplets, were presented repeatedly in fixed temporal order. On each trial the monkeys viewed three sequentially presented sample stimuli, followed by a test stimulus consisting of the same three images and a distractor image (chosen randomly from the remaining 27). The task was to touch the three images in their original order without touching the distractor. The most common error was touching the distractor when it had the same ordinal number (in its own triplet) as the correct image. Thus, the monkeys' natural tendency was to categorize images by their ordinal number. Additional, secondary strategies were used eventually to avoid the distractor images. These included memory of the sample images (working memory) and associations between sequence triplet members. Thus, monkeys use multiple mnemonic strategies according to their innate tendencies and the requirements of the task.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Terrace, H. The phylogeny and ontogeny of serial memory: List learning by pigeons and monkeys. Psychol. Sci. 4, 162– 169 (1993).
Ebbinghaus, H. Memory: A Contribution to Experimental Psychology (Dover, New York, 1964 (1885)).
Young, R. K. The stimulus in serial verbal learning. Am. J. Psychol. 74, 517–528 (1961).
Ebenholtz, S. in The Psychology of Learning and Motivation (ed. Bower, G.) 267– 314 (Academic, New York, 1972).
D'Amato, M. & Colombo, M. Representation of serial order in monkeys (Cebula apella). J. Exp. Psychol. Anim. Behav. Proc. 14, 131–139 ( 1988).
Terrace, H. Chunking by a pigeon in a serial learning task. Nature 325, 149–151 (1987).
Swartz, K., Chen, S. & Terrace, H. Serial learning by rhesus monkeys: I. Acquisition and retention of multiple four-item lists. J. Exp. Psychol. Anim. Behav. Proc. 17, 396–410 ( 1991).
McGonigle, B. & Chalmers, M. Monkeys are rational! Q. J. Exp. Psychol. 45, 189–228 (1992).
Treichler, F. & van Tilburg, D. Concurrent conditional discrimination tests of transitive inference by macaque monkeys: List linking. J. Exp. Psychol. Anim. Behav. Proc. 22, 105– 117 (1996).
Straub, R. O. & Terrace, H. S. Generalization of serial learning in the pigeon. Anim. Learn. Behav. 9, 454 –468 (1981).
Terrace, H. S. A non-verbal organism's knowledge of ordinal position in a serial learning task. J. Exp. Psychol. Anim. Behav. Proc. 41, 203–214 (1986).
Terrace, H., Chen, S. & Newman, A. Serial learning with a wild card by pigeons: Effect of list length. J. Comp. Psychol. 109, 162–172 (1995).
D'Amato, M. & Colombo, M. Serial learning with wild card items by monkeys (Cebus apella): implications for knowledge of ordinal position. J. Comp. Psychol. 103, 252– 263 (1989).
D'Amato, M. & Colombo, M. The symbolic distance effect in monkeys (Cebula apella). Anim. Learn. Behav. 18, 133–140 (1990).
Chen, S., Swartz, K. B. & Terrace, H. S. Knowledge of the ordinal position of list items in rhesus monkeys. Psychol. Sci. 8, 80– 86 (1997).
Sands, S. F. & Wright, A. A. Serial probe recognition performance by a rhesus monkey and a human with 10- and 20-item lists. J. Exp. Psychol. Anim. Behav. Proc. 6, 386– 396 (1980).
Gower, E. Short-term memory for the temporal order of events in monkeys. Behav. Brain Res. 52, 99–103 (1992).
Murray, E. I., Gaffan, D. & Mishkin, M. Neural substrates of visual stimulus-stimulus association in Rhesus monkeys. J. Neurosci. 13, 4549 –4561 (1993).
Sakai, K. & Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991).
Naya, Y., Sakai, K. & Miyashita, Y. Activity of primate infero-temporal neurons related to a sought target in pair-association task. Proc. Natl Acad. Sci. USA 93, 2664–2669 ( 1996).
Buffalo, B. & Gaffan, D. A primacy effect in monkeys when list position is relevant. Q. J. Exp. Psychol. 47B, 353–369 (1994).
Farrar, D. N. Picture memory in the chimpanzee. Percept. Motor Skills 25, 305–315 (1967).
Mishkin, M. A memory system in the monkey. Phil. Trans. R. Soc. Lond. 298, 83–95 (1982).
Fuster, J. The Prefrontal Cortex: Anatomy, Physiology and Neurophysiology of the Frontal Lobe (Raven, New York, 1989).
Colombo, M., Eickhoff, A. E. & Gross, C. G. The effects of inferior temporal and dorsolateral frontal lesions on serial-order behavior and visual imagery in monkeys. Cogn. Brain Res. 1, 211–217 (1993).
Petrides, M. Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey. J. Neurosci. 15, 359– 375 (1995).
Parker, A. & Gaffan, D. Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions. Neuropsychologia 36, 259 –271 (1998).
Acknowledgements
We thank D. Amit for insightful theoretical discussions and many practical suggestions during the course of these experiments, and S. Fusi, M. Dvorkin and O. Algaoy for computer assistance. This study was supported by grants from the Israel Science Foundation of the Academy of Arts and Sciences, the McDonnell-Pew Science Foundation and the US–Israel Binational Science Foundation (BSF). T.O. and V.Y. were supported in part by the Israel Ministry of Absorption.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Orlov, T., Yakovlev, V., Hochstein, S. et al. Macaque monkeys categorize images by their ordinal number. Nature 404, 77–80 (2000). https://doi.org/10.1038/35003571
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/35003571
This article is cited by
-
Uniquely human intelligence arose from expanded information capacity
Nature Reviews Psychology (2024)
-
Thinking about order: a review of common processing of magnitude and learned orders in animals
Animal Cognition (2023)
-
Mnemonic construction and representation of temporal structure in the hippocampal formation
Nature Communications (2022)
-
Zebra finches are able to learn affixation-like patterns
Animal Cognition (2016)
-
Ordinality and novel sequence learning in jackdaws
Animal Cognition (2012)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
