Animal Cognition

, Volume 12, Issue 5, pp 671–678 | Cite as

An analysis of immediate serial recall performance in a macaque

  • Matthew M. Botvinick
  • Jun Wang
  • Elizabeth Cowan
  • Stephane Roy
  • Christina Bastianen
  • J. Patrick Mayo
  • James C. Houk
Original Paper


There has been considerable research into the ability of nonhuman primates to process sequential information, a topic that is of interest in part because of the extensive involvement of sequence processing in human language use. Surprisingly, no previous study has unambiguously tested the ability of nonhuman primates to encode and immediately reproduce a novel temporal sequence of perceptual events, the ability tapped in the immediate serial recall (ISR) task extensively studied in humans. We report here the performance of a rhesus macaque on a spatial ISR task, closely resembling tasks widely used in human memory research. Detailed analysis of the monkey’s recall performance indicates a number of important parallels with human ISR, consistent with the idea that a single mechanism for short-term serial order memory may be shared across species.


Serial order Macaque Working memory 



Portions of the work reported were supported by the National Institutes of Health, grants NS44837 (JCH), P01-NS44383 (JCH) and MH16804 (MMB).


  1. Avons SE, Wright KL, Pammer K (1994) The word-length effect in probed and serial recall. Q J Exp Psychol 47A:207–231Google Scholar
  2. Baddeley AD (2003) Working memory and language: a review. J Commun Disord 36:189–208PubMedCrossRefGoogle Scholar
  3. Barone P, Joseph JP (1989) Prefrontal cortex and spatial sequencing in macaque monkey. Exp Brain Res 78:447–464PubMedCrossRefGoogle Scholar
  4. Bjork EL, Healy AF (1974) Short-term order and item retention. J Verbal Learn Verbal Behav 13:80–97CrossRefGoogle Scholar
  5. Bjork RA, Whitten WB (1974) Recency-sensitive retrieval processes in long-term free recall. Cogn Psychol 6:173–189CrossRefGoogle Scholar
  6. Botvinick M, Watanabe T (2007) From numerosity to ordinal rank: a gain-field model of serial order representation in cortical working memory. J Neurosci 27:8636–8642PubMedCrossRefGoogle Scholar
  7. Brown G, Preece T, Hulme C (2000) Oscillator-based memory for serial order. Psychol Rev 107:127–181PubMedCrossRefGoogle Scholar
  8. Buchanan JP, Gill TV, Braggio JT (1981) Serial position and clustering effects in a chimpanzee’s “free recall”. Mem Cognit 9:651–660PubMedGoogle Scholar
  9. Burgess N, Hitch GJ (1999) Memory for serial order: a network model of the phonological loop and its timing. Psychol Rev 106:551–581CrossRefGoogle Scholar
  10. Castro CA, Larsen T (1992) Primacy and recency effects in nonhuman primates. J Exp Psychol Anim Behav Process 18:335–340PubMedCrossRefGoogle Scholar
  11. Chen S, Swartz KB, Terrace HS (1997) Knowledge of the ordinal position of list items in rhesus monkeys. Psychol Sci 8:80–86CrossRefGoogle Scholar
  12. Conrad R (1960) Serial order intrusions in immediate memory. Br J Psychol 51:45–48PubMedGoogle Scholar
  13. Conrad R, Hull AJ (1964) Information, acoustic confusion and memory span. Br J Psychol 55:429–432PubMedGoogle Scholar
  14. Conway CM, Christiansen MH (2001) Sequential learning in non-human primates. Trends Cogn Sci 5:539–546PubMedCrossRefGoogle Scholar
  15. Crannell CW, Parrish JM (1957) A comparison of immediate memory span for digits, letters, and words. J Psychol 44:319–327Google Scholar
  16. Crowder RG, Morton J (1969) Precategorical acoustic storage. Percept Psychophys 5:365–373Google Scholar
  17. Drewnowski A, Murdock BBJ (1980) The role of auditory features in memory span for words. J Exp Psychol Learn Mem Cogn 6:319–332Google Scholar
  18. Farrand P, Jones D (1996) Direction of report in spatial and verbal serial short-term memory. Q J Exp Psychol 49:140–158CrossRefGoogle Scholar
  19. Farrand P, Parmentier FBR, Jones DM (2001) Temporal-spatial memory: retrieval of spatial information does not reduce recency. Acta Psychol 106:285–301CrossRefGoogle Scholar
  20. Fischer MH (2001) Probing spatial working memory with the Corsi blocks task. Brain Cogn 45:143–154PubMedCrossRefGoogle Scholar
  21. Fitch WT, Hauser MD (2004) Computational constraints on syntactic processing in a nonhuman primate. Science 16:377–380CrossRefGoogle Scholar
  22. Fraser D, Park S, Clark G, Yohanna D, Houk JC (2004) Spatial serial order processing in schizophrenia. Schizophr Res 70:203–213PubMedCrossRefGoogle Scholar
  23. Funahashi S, Inoue M, Kubota K (1997) Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation. Behav Brain Res 84:203–223PubMedCrossRefGoogle Scholar
  24. Graybiel AM (1998) The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem 70:119–136PubMedCrossRefGoogle Scholar
  25. Henson RNA (1996) Short-term memory for serial order. University of Cambridge, CambridgeGoogle Scholar
  26. Henson RNA (1998) Short-term memory for serial order: the start-end model. Cogn Psychol 36:73–137PubMedCrossRefGoogle Scholar
  27. Henson RNA, Norris D, Page M, Baddeley AD (1996) Unchained memory: error patterns rule out chaining models of immediate serial recall. Q J Exp Psychol 49A:80–115CrossRefGoogle Scholar
  28. Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, Doya K (1999) Parallel neural networks for learning sequential behaviors. Trends Neurosci 22:464–471PubMedCrossRefGoogle Scholar
  29. Hitch GJ (1974) Short-term memory for spatial and temporal information. Q J Exp Psychol 26:503–513PubMedCrossRefGoogle Scholar
  30. Hitch GJ, Fastame MC, Flude B (2005) How is serial order of a verbal sequence coded? Some comparison between models. Memory 13:247–258PubMedCrossRefGoogle Scholar
  31. Inoue S, Matsuzawa T (2007) Working memory of numerals in chimpanzees. Curr Biol 17:1004–1005CrossRefGoogle Scholar
  32. Jahnke JC (1963) Serial position effects in immediate serial recall. J Verbal Learn Verbal Behav 2:284–287CrossRefGoogle Scholar
  33. Jahnke JC (1965) Primacy and recency effects in serial-position curves of immediate recall. J Exp Psychol 70:130–132PubMedCrossRefGoogle Scholar
  34. Jones D, Farrand P, Stuart G, Morris N (1995) Functional equivalence of verbal and spatial information in serial short-term memory. J Exp Psychol Learn Mem Cogn 21:1008–1018PubMedCrossRefGoogle Scholar
  35. Kawai N, Matsuzawa T (2000) Numerical memory span in a chimpanzee. Nature 403:39–40PubMedCrossRefGoogle Scholar
  36. Kesner RP, Novak JM (1982) Serial position curve in rats: role of dorsal hippocampus. Science 218:173–175PubMedCrossRefGoogle Scholar
  37. Korsnes MS, Magnussen S (1996) Age comparisons of serial position effects in short-term memory. Acta Psychol 94:133–143CrossRefGoogle Scholar
  38. Martin N, Gupta P (2004) Exploring the relationship between word processing and verbal short-term memory: evidence from associations and dissociations. Cogn Neuropsychol 21:213–228CrossRefGoogle Scholar
  39. Matzke SM, Castro CA (1998) Primacy and recency effects in rhesus monkeys (Macaca mulatta) using a serial probe recognition task III. A developmental analysis. Dev Psychobiol 32:215–224PubMedCrossRefGoogle Scholar
  40. McFarland DJ, Cacace AT (1995) Comparisons of memory for nonverbal auditory and visual sequential stimuli. Psychol Res 57:80–87PubMedGoogle Scholar
  41. Ninokura Y, Mushiake H, Tanji J (2003) Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. J Neurophysiol 89:2868–2873PubMedCrossRefGoogle Scholar
  42. Orlov T, Kakovlev V, Hochstein S, Zohary E (2000) Macaque monkeys categorize images by their ordinal number. Nature 404:77–80PubMedCrossRefGoogle Scholar
  43. Page M, Norris D (1998) The primacy model: a new model of immediate serial recall. Psychol Rev 105:761–781PubMedCrossRefGoogle Scholar
  44. Petrides M (1991) Functional specialization within the dorsolateral frontal cortex for serial order memory. Proc Biol Sci 246:299–306PubMedCrossRefGoogle Scholar
  45. Smyth MM, Scholey KA (1996) Serial order in spatial immediate memory. Q J Exp Psychol 49A:159–177CrossRefGoogle Scholar
  46. Surprenant AM, Kelley MR, Farley LA, Neath I (2005) Fill-in and infill errors in order memory. Memory 13:267–273PubMedCrossRefGoogle Scholar
  47. Terrace HS (2005) The simultaneous chain: a new approach to serial learning. Trends Cogn Sci 9:202–210PubMedCrossRefGoogle Scholar
  48. Wright AA (1998) Auditory list memory in rhesus monkeys. Psychol Sci 9:91–98CrossRefGoogle Scholar
  49. Wright AA, Roediger HL (2003) Interference processes in monkey auditory list memory. Psychon Bull Rev 10:696–702PubMedGoogle Scholar
  50. Wright AA, Santiago HC, Sands SF (1984) Monkey memory: same/different concept learning, serial probe acquisition, and probe delay effects. J Exp Psychol Anim Behav Process 10:513–529PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Matthew M. Botvinick
    • 1
  • Jun Wang
    • 2
  • Elizabeth Cowan
    • 2
  • Stephane Roy
    • 2
  • Christina Bastianen
    • 2
  • J. Patrick Mayo
    • 3
  • James C. Houk
    • 2
  1. 1.Department of Psychology and Princeton Neuroscience InstitutePrinceton UniversityPrincetonUSA
  2. 2.Department of Physiology, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  3. 3.Department of Neuroscience, Center for Neuroscience and Center for the Neural Basis of CognitionUniversity of PittsburghPittsburghUSA

Personalised recommendations