Skip to main content
Journal of the Experimental Analysis of Behavior logoLink to Journal of the Experimental Analysis of Behavior
. 1999 Mar;71(2):215–251. doi: 10.1901/jeab.1999.71-215

Time and memory: towards a pacemaker-free theory of interval timing.

J E Staddon 1, J J Higa 1
PMCID: PMC1284701  PMID: 10220931

Abstract

A popular view of interval timing in animals is that it is driven by a discrete pacemaker-accumulator mechanism that yields a linear scale for encoded time. But these mechanisms are fundamentally at odds with the Weber law property of interval timing, and experiments that support linear encoded time can be interpreted in other ways. We argue that the dominant pacemaker-accumulator theory, scalar expectancy theory (SET), fails to explain some basic properties of operant behavior on interval-timing procedures and can only accommodate a number of discrepancies by modifications and elaborations that raise questions about the entire theory. We propose an alternative that is based on principles of memory dynamics derived from the multiple-time-scale (MTS) model of habituation. The MTS timing model can account for data from a wide variety of time-related experiments: proportional and Weber law temporal discrimination, transient as well as persistent effects of reinforcement omission and reinforcement magnitude, bisection, the discrimination of relative as well as absolute duration, and the choose-short effect and its analogue in number-discrimination experiments. Resemblances between timing and counting are an automatic consequence of the model. We also argue that the transient and persistent effects of drugs on time estimates can be interpreted as well within MTS theory as in SET. Recent real-time physiological data conform in surprising detail to the assumptions of the MTS habituation model. Comparisons between the two views suggest a number of novel experiments.

Full Text

The Full Text of this article is available as a PDF (326.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bonem M., Crossman E. K. Elucidating the effects of reinforcement magnitude. Psychol Bull. 1988 Nov;104(3):348–362. doi: 10.1037/0033-2909.104.3.348. [DOI] [PubMed] [Google Scholar]
  2. Brunner D., Fairhurst S., Stolovitzky G., Gibbon J. Mnemonics for variability: remembering food delay. J Exp Psychol Anim Behav Process. 1997 Jan;23(1):68–83. doi: 10.1037//0097-7403.23.1.68. [DOI] [PubMed] [Google Scholar]
  3. Brunner D., Gibbon J., Fairhurst S. Choice between fixed and variable delays with different reward amounts. J Exp Psychol Anim Behav Process. 1994 Oct;20(4):331–346. [PubMed] [Google Scholar]
  4. Byrne J. H. Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J Neurophysiol. 1982 Aug;48(2):431–438. doi: 10.1152/jn.1982.48.2.431. [DOI] [PubMed] [Google Scholar]
  5. CASTER W. O., AHN P. Electrocardiographic notching in rats deficient in essential fatty acids. Science. 1963 Mar 22;139(3560):1213–1213. doi: 10.1126/science.139.3560.1213. [DOI] [PubMed] [Google Scholar]
  6. Carew T. J., Pinsker H. M., Kandel E. R. Long-term habituation of a defensive withdrawal reflex in aplysia. Science. 1972 Jan 28;175(4020):451–454. doi: 10.1126/science.175.4020.451. [DOI] [PubMed] [Google Scholar]
  7. Chung S. H., Herrnstein R. J. Choice and delay of reinforcement. J Exp Anal Behav. 1967 Jan;10(1):67–74. doi: 10.1901/jeab.1967.10-67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Church R. M., Deluty M. Z. Bisection of temporal intervals. J Exp Psychol Anim Behav Process. 1977 Jul;3(3):216–228. doi: 10.1037//0097-7403.3.3.216. [DOI] [PubMed] [Google Scholar]
  9. Church R. M., Gibbon J. Temporal generalization. J Exp Psychol Anim Behav Process. 1982 Apr;8(2):165–186. [PubMed] [Google Scholar]
  10. Church R. M., Meck W. H., Gibbon J. Application of scalar timing theory to individual trials. J Exp Psychol Anim Behav Process. 1994 Apr;20(2):135–155. doi: 10.1037//0097-7403.20.2.135. [DOI] [PubMed] [Google Scholar]
  11. Davis M. Effects of interstimulus interval length and variability on startle-response habituation in the rat. J Comp Physiol Psychol. 1970 Aug;72(2):177–192. doi: 10.1037/h0029472. [DOI] [PubMed] [Google Scholar]
  12. Dreyfus L. R., Fetterman J. G., Smith L. D., Stubbs D. A. Discrimination of temporal relations by pigeons. J Exp Psychol Anim Behav Process. 1988 Oct;14(4):349–367. [PubMed] [Google Scholar]
  13. EKMAN G. IS THE POWER LAW A SPECIAL CASE OF FECHNER'S LAW? Percept Mot Skills. 1964 Dec;19:730–730. doi: 10.2466/pms.1964.19.3.730. [DOI] [PubMed] [Google Scholar]
  14. Fetterman J. G. A temporal intermediate stimulus problem. J Exp Psychol Anim Behav Process. 1998 Oct;24(4):379–395. doi: 10.1037//0097-7403.24.4.379. [DOI] [PubMed] [Google Scholar]
  15. Fetterman J. G., Dreyfus L. R., Stubbs D. A. Discrimination of duration ratios. J Exp Psychol Anim Behav Process. 1989 Jul;15(3):253–263. [PubMed] [Google Scholar]
  16. Fetterman J. G., MacEwen D. Short-term memory for responses: the "choose-small" effect. J Exp Anal Behav. 1989 Nov;52(3):311–324. doi: 10.1901/jeab.1989.52-311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gibbon J., Church R. M. Comparison of variance and covariance patterns in parallel and serial theories of timing. J Exp Anal Behav. 1992 May;57(3):393–406. doi: 10.1901/jeab.1992.57-393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gibbon J., Church R. M. Representation of time. Cognition. 1990 Nov;37(1-2):23–54. doi: 10.1016/0010-0277(90)90017-e. [DOI] [PubMed] [Google Scholar]
  19. Gibbon J., Malapani C., Dale C. L., Gallistel C. Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol. 1997 Apr;7(2):170–184. doi: 10.1016/s0959-4388(97)80005-0. [DOI] [PubMed] [Google Scholar]
  20. Gingrich K. J., Byrne J. H. Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J Neurophysiol. 1985 Mar;53(3):652–669. doi: 10.1152/jn.1985.53.3.652. [DOI] [PubMed] [Google Scholar]
  21. Glantz J. Magnetic brain imaging traces a stairway to memory. Science. 1998 Apr 3;280(5360):37–37. doi: 10.1126/science.280.5360.37. [DOI] [PubMed] [Google Scholar]
  22. Hinson J. M., Staddon J. E. Hill-climbing by pigeons. J Exp Anal Behav. 1983 Jan;39(1):25–47. doi: 10.1901/jeab.1983.39-25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Innis N. K., Staddon J. E. Temporal tracking on cyclic-interval reinforcement schedules. J Exp Anal Behav. 1971 Nov;16(3):411–423. doi: 10.1901/jeab.1971.16-411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Killeen P. R., Fetterman J. G. A behavioral theory of timing. Psychol Rev. 1988 Apr;95(2):274–295. doi: 10.1037/0033-295x.95.2.274. [DOI] [PubMed] [Google Scholar]
  25. Killeen P. R., Fetterman J. G. The behavioral theory of timing: transition analyses. J Exp Anal Behav. 1993 Mar;59(2):411–422. doi: 10.1901/jeab.1993.59-411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kondo T., Mori T., Lebedeva N. V., Aoki S., Ishiura M., Golden S. S. Circadian rhythms in rapidly dividing cyanobacteria. Science. 1997 Jan 10;275(5297):224–227. doi: 10.1126/science.275.5297.224. [DOI] [PubMed] [Google Scholar]
  27. Leak T. M., Gibbon J. Simultaneous timing of multiple intervals: implications of the scalar property. J Exp Psychol Anim Behav Process. 1995 Jan;21(1):3–19. [PubMed] [Google Scholar]
  28. Lejeune H., Ferrara A., Simons F., Wearden J. H. Adjusting to changes in the time of reinforcement: peak-interval transitions in rats. J Exp Psychol Anim Behav Process. 1997 Apr;23(2):211–231. doi: 10.1037//0097-7403.23.2.211. [DOI] [PubMed] [Google Scholar]
  29. Lowe C. F., Davey G. C., Harzem P. Effects of reinforcement magnitude on interval and ratio schedules. J Exp Anal Behav. 1974 Nov;22(3):553–560. doi: 10.1901/jeab.1974.22-553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Meck W. H., Church R. M., Gibbon J. Temporal integration in duration and number discrimination. J Exp Psychol Anim Behav Process. 1985 Oct;11(4):591–597. [PubMed] [Google Scholar]
  31. Meck W. H. Neuropharmacology of timing and time perception. Brain Res Cogn Brain Res. 1996 Jun;3(3-4):227–242. doi: 10.1016/0926-6410(96)00009-2. [DOI] [PubMed] [Google Scholar]
  32. Meck W. H. Selective adjustment of the speed of internal clock and memory processes. J Exp Psychol Anim Behav Process. 1983 Apr;9(2):171–201. [PubMed] [Google Scholar]
  33. Perone M., Courtney K. Fixed-ratio pausing: Joint effects of past reinforcer magnitude and stimuli correlated with upcoming magnitude. J Exp Anal Behav. 1992 Jan;57(1):33–46. doi: 10.1901/jeab.1992.57-33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. ROZIN P. TEMPERATURE INDEPENDENCE OF AN ARBITRARY TEMPORAL DISCRIMINATION IN THE GOLDFISH. Science. 1965 Jul 30;149(3683):561–563. doi: 10.1126/science.149.3683.561. [DOI] [PubMed] [Google Scholar]
  35. Roberts S., Holder M. D. What starts an internal clock? J Exp Psychol Anim Behav Process. 1984 Jul;10(3):273–296. [PubMed] [Google Scholar]
  36. STADDON J. E. SOME PROPERTIES OF SPACED RESPONDING IN PIGEONS. J Exp Anal Behav. 1965 Jan;8:19–27. doi: 10.1901/jeab.1965.8-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shull R. L., Mellon R. C., Sharp J. A. Delay and number of food reinforcers: Effects on choice and latencies. J Exp Anal Behav. 1990 Mar;53(2):235–246. doi: 10.1901/jeab.1990.53-235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Spitzer N. C., Sejnowski T. J. Biological information processing: bits of progress. Science. 1997 Aug 22;277(5329):1060–1061. doi: 10.1126/science.277.5329.1060. [DOI] [PubMed] [Google Scholar]
  39. Staddon J. E. A note on behavioural contrast and frustation. Q J Exp Psychol. 1974 May;26(2):285–292. doi: 10.1080/14640747408400414. [DOI] [PubMed] [Google Scholar]
  40. Staddon J. E. Effect of reinforcement duration on fixed-interval responding. J Exp Anal Behav. 1970 Jan;13(1):9–11. doi: 10.1901/jeab.1970.13-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Staddon J. E., Higa J. J. Multiple time scales in simple habituation. Psychol Rev. 1996 Oct;103(4):720–733. doi: 10.1037/0033-295x.103.4.720. [DOI] [PubMed] [Google Scholar]
  42. Staddon J. E., Innis N. K. Reinforcement omission on fixed-interval schedules. J Exp Anal Behav. 1969 Sep;12(5):689–700. doi: 10.1901/jeab.1969.12-689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Staddon J. E. Multiple fixed-interval schedules: transient contrast and temporal inhibition. J Exp Anal Behav. 1969 Jul;12(4):583–590. doi: 10.1901/jeab.1969.12-583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Staddon J. E. Reinforcement omission on temporal go-no-go schedules. J Exp Anal Behav. 1972 Sep;18(2):223–229. doi: 10.1901/jeab.1972.18-223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Starr B. C., Staddon J. E. Temporal control of periodic schedules: signal properties of reinforcement and blackout. J Exp Anal Behav. 1974 Nov;22(3):535–545. doi: 10.1901/jeab.1974.22-535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Stubbs A. The discrimination of stimulus duration by pigeons. J Exp Anal Behav. 1968 May;11(3):223–238. doi: 10.1901/jeab.1968.11-223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Stubbs D. A., Dreyfus L. R., Fetterman J. G., Boynton D. M., Locklin N., Smith L. D. Duration comparison: relative stimulus differences stimulus age, and stimulus predictiveness. J Exp Anal Behav. 1994 Jul;62(1):15–32. doi: 10.1901/jeab.1994.62-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Thompson R. F., Spencer W. A. Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev. 1966 Jan;73(1):16–43. doi: 10.1037/h0022681. [DOI] [PubMed] [Google Scholar]
  49. Wixted J. T., Ebbesen E. B. Genuine power curves in forgetting: a quantitative analysis of individual subject forgetting functions. Mem Cognit. 1997 Sep;25(5):731–739. doi: 10.3758/bf03211316. [DOI] [PubMed] [Google Scholar]
  50. Wynne C. D., Staddon J. E. Typical delay determines waiting time on periodic-food schedules: Static and dynamic tests. J Exp Anal Behav. 1988 Sep;50(2):197–210. doi: 10.1901/jeab.1988.50-197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Zeiler M. D., Powell D. G. Temporal control in fixed-interval schedules. J Exp Anal Behav. 1994 Jan;61(1):1–9. doi: 10.1901/jeab.1994.61-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of the Experimental Analysis of Behavior are provided here courtesy of Society for the Experimental Analysis of Behavior

RESOURCES