Skip to main content
SpringerLink
Log in

Searching for the Holy Grail: Temporally Informative Firing Patterns in the Rat

  • Chapter
  • First Online:
Neurobiology of Interval Timing

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 829))

Abstract

This chapter reviews our work from the past decade investigating cortical and striatal firing patterns in rats while they time intervals in the multi-seconds range. We have found that both cortical and striatal firing rates contain information that the rat can use to identify how much time has elapsed both from trial onset and from the onset of an active response state. I describe findings showing that the striatal neurons that are modulated by time are also modulated by overt behaviors, suggesting that time modulates the strength of motor coding in the striatum, rather than being represented as an abstract quantity in isolation. I also describe work showing that there are a variety of temporally informative activity patterns in pre-motor cortex, and argue that the heterogeneity of these patterns can enhance an organism’s temporal estimate. Finally, I describe recent behavioral work from my lab in which the simultaneous cueing of multiple durations leads to a scalar temporal expectation at an intermediate time, providing strong support for a monotonic representation of time.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Henderson J, Hurly TA, Bateson M, Healy SD. Timing in free-living rufous hummingbirds, Selasphorus rufus. Curr Biol. 2006;16(5):512–5.

    Article  PubMed  CAS  Google Scholar 

  2. Bateson M. Currencies for decision making: the foraging starling as a model animal. Oxford: Oxford University Press; 1993.

    Google Scholar 

  3. Gallistel CR, Gibbon J. Time, rate, and conditioning. Psychol Rev. 2000;107(2):289–344.

    Article  PubMed  CAS  Google Scholar 

  4. Miller RR, Barnet RC. The role of time in elementary associations. Curr Dir Psychol Sci. 1993;2(4):106–11.

    Article  Google Scholar 

  5. Meck WH. Selective adjustment of the speed of internal clock and memory processes. J Exp Psychol. 1983;9(2):171–201.

    CAS  Google Scholar 

  6. Matell MS, Bateson M, Meck WH. Single-trials analyses demonstrate that increases in clock speed contribute to the methamphetamine-induced horizontal shifts in peak-interval timing functions. Psychopharmacology (Berl). 2006;188(2):201–12. Epub 2006/08/29.

    Article  CAS  Google Scholar 

  7. Buhusi CV, Meck WH. Differential effects of methamphetamine and haloperidol on the control of an internal clock. Behav Neurosci. 2002;116(2):291–7.

    Article  PubMed  CAS  Google Scholar 

  8. Meck WH. Neuroanatomical localization of an internal clock: a functional link between mesolimbic, nigrostriatal, and mesocortical dopaminergic systems. Brain Res. 2006;1109:93–107.

    Article  PubMed  CAS  Google Scholar 

  9. Galtress T, Kirkpatrick K. The role of the nucleus accumbens core in impulsive choice, timing, and reward processing. Behav Neurosci. 2010;124(1):26–43. Epub 2010/02/10.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Harrington DL, Haaland KY. Neural underpinnings of temporal processing: a review of focal lesion, pharmacological, and functional imaging research. Rev Neurosci. 1999;10(2):91–116.

    Article  PubMed  CAS  Google Scholar 

  11. Gooch CM, Wiener M, Hamilton AC, Coslett HB. Temporal discrimination of sub- and suprasecond time intervals: a voxel-based lesion mapping analysis. Front Integr Neurosci. 2011;5:59. Epub 2011/10/21.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Coull JT. fMRI studies of temporal attention: allocating attention within, or towards, time. Brain Res Cogn Brain Res. 2004;21(2):216–26.

    Article  PubMed  Google Scholar 

  13. Ferrandez AM, Hugueville L, Lehericy S, Poline JB, Marsault C, Pouthas V. Basal ganglia and supplementary motor area subtend duration perception: an fMRI study. Neuroimage. 2003;19(4):1532–44.

    Article  PubMed  CAS  Google Scholar 

  14. Lewis PA, Miall RC. Brain activation patterns during measurement of sub- and supra-second intervals. Neuropsychologia. 2003;41(12):1583–92.

    Article  PubMed  CAS  Google Scholar 

  15. Wiener M, Turkeltaub P, Coslett HB. The image of time: a voxel-wise meta-analysis. Neuroimage. 2010;49(2):1728–40. Epub 2009/10/06.

    Article  PubMed  Google Scholar 

  16. Drew MR, Simpson EH, Kellendonk C, Herzberg WG, Lipatova O, Fairhurst S, et al. Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci. 2007;27(29):7731–9. Epub 2007/07/20.

    Article  PubMed  CAS  Google Scholar 

  17. Wiener M, Lohoff FW, Coslett HB. Double dissociation of dopamine genes and timing in humans. J Cogn Neurosci. 2011;23(10):2811–21. Epub 2011/01/26.

    Article  PubMed  Google Scholar 

  18. Fuster JM, Alexander GE. Neuron activity related to short-term memory. Science. 1971;173(3997):652–4. Epub 1971/08/13.

    Article  PubMed  CAS  Google Scholar 

  19. Kubota K, Niki H. Prefrontal cortical unit activity and delayed alternation performance in monkeys. J Neurophysiol. 1971;34(3):337–47. Epub 1971/05/01.

    PubMed  CAS  Google Scholar 

  20. Romo R, Brody CD, Hernandez A, Lemus L. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature. 1999;399(6735):470–3.

    Article  PubMed  CAS  Google Scholar 

  21. Prut Y, Vaadia E, Bergman H, Haalman I, Slovin H, Abeles M. Spatiotemporal structure of cortical activity: properties and behavioral relevance. J Neurophysiol. 1998;79(6):2857–74.

    PubMed  CAS  Google Scholar 

  22. Kojima S, Goldman-Rakic PS. Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response. Brain Res. 1982;248(1):43–9.

    Article  PubMed  CAS  Google Scholar 

  23. Genovesio A, Tsujimoto S, Wise SP. Feature- and order-based timing representations in the frontal cortex. Neuron. 2009;63(2):254–66. Epub 2009/07/31.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  24. Mita A, Mushiake H, Shima K, Matsuzaka Y, Tanji J. Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat Neurosci. 2009;12(4):502–7. Epub 2009/03/03.

    Article  PubMed  CAS  Google Scholar 

  25. Janssen P, Shadlen MN. A representation of the hazard rate of elapsed time in macaque area LIP. Nat Neurosci. 2005;8(2):234–41.

    Article  PubMed  CAS  Google Scholar 

  26. Brody CD, Hernandez A, Zainos A, Romo R. Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb Cortex. 2003;13(11):1196–207.

    Article  PubMed  Google Scholar 

  27. Leon MI, Shadlen MN. Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron. 2003;38(2):317–27.

    Article  PubMed  CAS  Google Scholar 

  28. Merchant H, Zarco W, Perez O, Prado L, Bartolo R. Measuring time with different neural chronometers during a synchronization-continuation task. Proc Natl Acad Sci U S A. 2011;108(49):19784–9. Epub 2011/11/23.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Chiba A, Oshio K, Inase M. Striatal neurons encoded temporal information in duration discrimination task. Exp Brain Res. 2008;186(4):671–6. Epub 2008/03/19.

    Article  PubMed  Google Scholar 

  30. Oshio K, Chiba A, Inase M. Temporal filtering by prefrontal neurons in duration discrimination. Eur J Neurosci. 2008;28(11):2333–43. Epub 2008/11/21.

    Article  PubMed  Google Scholar 

  31. Oshio K, Chiba A, Inase M. Delay period activity of monkey prefrontal neurones during duration-discrimination task. Eur J Neurosci. 2006;23(10):2779–90. Epub 2006/07/05.

    Article  PubMed  Google Scholar 

  32. Roberts S. Isolation of an internal clock. J Exp Psychol Anim Behav Process. 1981;7(3):242–68. Epub 1981/07/01.

    Article  PubMed  CAS  Google Scholar 

  33. Church RM, Deluty HZ. The bisection of temporal intervals. J Exp Psychol Anim Behav Process. 1977;3:216–28.

    Article  PubMed  CAS  Google Scholar 

  34. Fetterman JG, Killeen PR, Hall S. Watching the clock. Behav Processes. 1998;44(2):211–24.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Killeen PR, Weiss NA. Optimal timing and the Weber function. Psychol Rev. 1987;94(4):455–68.

    Article  PubMed  CAS  Google Scholar 

  36. Rakitin BC, Gibbon J, Penney TB, Malapani C, Hinton SC, Meck WH. Scalar expectancy theory and peak-interval timing in humans. J Exp Psychol Anim Behav Process. 1998;24(1):15–33.

    Article  PubMed  CAS  Google Scholar 

  37. Aldridge JW, Berridge KC. Coding of serial order by neostriatal neurons: a “natural action” approach to movement sequence. J Neurosci. 1998;18(7):2777–87.

    PubMed  CAS  Google Scholar 

  38. Green L, Myerson J. A discounting framework for choice with delayed and probabilistic rewards. Psychol Bull. 2004;130(5):769–92. Epub 2004/09/16.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Gibbon J. Scalar expectancy theory and Weber’s law in animal timing. Psychol Rev. 1977;84:279–325.

    Article  Google Scholar 

  40. Wearden JH. Do humans possess an internal clock with scalar properties. Learn Motiv. 1991;22:59–83.

    Article  Google Scholar 

  41. Buhusi CV, Meck WH. What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci. 2005;6:755–65.

    Article  PubMed  CAS  Google Scholar 

  42. Taylor KM, Horvitz JC, Balsam PD. Amphetamine affects the start of responding in the peak interval timing task. Behav Processes. 2007;74(2):168–75. Epub 2007/01/16.

    Article  PubMed  Google Scholar 

  43. Gallistel CR, Fairhurst S, Balsam P. The learning curve: implications of a quantitative analysis. Proc Natl Acad Sci U S A. 2004;101(36):13124–31. Epub 2004/08/28.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Galtress T, Marshall AT, Kirkpatrick K. Motivation and timing: clues for modeling the reward system. Behav Processes. 2012;90(1):142–53. Epub 2012/03/17.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Matell MS, Meck WH, Nicolelis MA. Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. Behav Neurosci. 2003;117(4):760–73.

    Article  PubMed  Google Scholar 

  46. Matell MS, Meck WH. Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Res Cogn Brain Res. 2004;21(2):139–70.

    Article  PubMed  Google Scholar 

  47. Matell MS, Meck WH. Neuropsychological mechanisms of interval timing behavior. Bioessays. 2000;22(1):94–103.

    Article  PubMed  CAS  Google Scholar 

  48. Groves PM, Garcia-Munoz M, Linder JC, Manley MS, Martone ME, Young SJ. Elements of the intrinsic organization and information processing in the neostriatum. In: Houk JC, Davis JL, Beiser DG, editors. Models of information processing in the basal ganglia. Cambridge: MIT Press; 1995. p. 51–96.

    Google Scholar 

  49. Houk JC. Information processing in modular circuits linking basal ganglia and cerebral cortex. In: Houk JC, Davis JL, Beiser DG, editors. Models of information processing in the basal ganglia. Cambridge: MIT Press; 1995. p. 3–10.

    Google Scholar 

  50. Gooch CM, Wiener M, Portugal GS, Matell MS. Evidence for separate neural mechanisms for the timing of discrete and sustained responses. Brain Res. 2007;1156:139–51.

    Article  PubMed  CAS  Google Scholar 

  51. Matell MS, Portugal GS. Impulsive responding on the peak-interval procedure. Behav Processes. 2007;74:198–208 (special issue in tribute to Russell Church).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Portugal GS, Wilson AG, Matell MS. Behavioral sensitivity of temporally modulated striatal neurons. Front Integr Neurosci. 2011;5:30. Epub 2011/08/03.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Harrington DL, Haaland KY, Hermanowicz N. Temporal processing in the basal ganglia. Neuropsychology. 1998;12(1):3–12.

    Article  PubMed  CAS  Google Scholar 

  54. Livesey AC, Wall MB, Smith AT. Time perception: manipulation of task difficulty dissociates clock functions from other cognitive demands. Neuropsychologia. 2007;45(2):321–31.

    Article  PubMed  Google Scholar 

  55. Parent A, Hazrati LN. Anatomical aspects of information processing in primate basal ganglia. Trends Neurosci. 1993;16(3):111–6.

    Article  PubMed  CAS  Google Scholar 

  56. Schultz W. The phasic reward signal of primate dopamine neurons. Adv Pharmacol. 1998;42:686–90.

    Article  PubMed  CAS  Google Scholar 

  57. Hollerman JR, Schultz W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci. 1998;1(4):304–9.

    Article  PubMed  CAS  Google Scholar 

  58. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science. 1997;275(5306):1593–9.

    Article  PubMed  CAS  Google Scholar 

  59. Fiorillo CD, Tobler PN, Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science. 2003;299(5614):1898–902.

    Article  PubMed  CAS  Google Scholar 

  60. Alexander GE, Crutcher MD, DeLong MR. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res. 1990;85:119–46.

    Article  PubMed  CAS  Google Scholar 

  61. Coull J, Nobre A. Dissociating explicit timing from temporal expectation with fMRI. Curr Opin Neurobiol. 2008;18(2):137–44. Epub 2008/08/12.

    Article  PubMed  CAS  Google Scholar 

  62. Wiener M, Matell MS, Coslett HB. Multiple mechanisms for temporal processing. Front Integr Neurosci. 2011;5:31. Epub 2011/08/03.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Ivry RB, Spencer RM. The neural representation of time. Curr Opin Neurobiol. 2004;14(2):225–32.

    Article  PubMed  CAS  Google Scholar 

  64. Rao SM, Mayer AR, Harrington DL. The evolution of brain activation during temporal processing. Nat Neurosci. 2001;4(3):317–23.

    Article  PubMed  CAS  Google Scholar 

  65. Lucchetti C, Ulrici A, Bon L. Dorsal premotor areas of nonhuman primate: functional flexibility in time domain. Eur J Appl Physiol. 2005;95(2–3):121–30. Epub 2005/07/28.

    Article  PubMed  Google Scholar 

  66. Roesch MR, Olson CR. Neuronal activity dependent on anticipated and elapsed delay in macaque prefrontal cortex, frontal and supplementary eye fields, and premotor cortex. J Neurophysiol. 2005;94(2):1469–97.

    Article  PubMed  Google Scholar 

  67. Hernandez A, Zainos A, Romo R. Temporal evolution of a decision-making process in medial premotor cortex. Neuron. 2002;33(6):959–72.

    Article  PubMed  CAS  Google Scholar 

  68. Macar F, Anton JL, Bonnet M, Vidal F. Timing functions of the supplementary motor area: an event-related fMRI study. Brain Res Cogn Brain Res. 2004;21(2):206–15.

    Article  PubMed  Google Scholar 

  69. Macar F, Vidal F, Casini L. The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes. Exp Brain Res. 1999;125(3):271–80.

    Article  PubMed  CAS  Google Scholar 

  70. Matell MS, Shea-Brown E, Gooch C, Wilson AG, Rinzel J. A heterogeneous population code for elapsed time in rat medial agranular cortex. Behav Neurosci. 2011;125(1):54–73. Epub 2011/02/16.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Reep RL, Cheatwood JL, Corwin JV. The associative striatum: organization of cortical projections to the dorsocentral striatum in rats. J Comp Neurol. 2003;467(3):271–92.

    Article  PubMed  Google Scholar 

  72. Reep RL, Corwin JV. Topographic organization of the striatal and thalamic connections of rat medial agranular cortex. Brain Res. 1999;841(1–2):43–52.

    Article  PubMed  CAS  Google Scholar 

  73. Church RM, Meck WH, Gibbon J. Application of scalar timing theory to individual trials. J Exp Psychol Anim Behav Process. 1994;20(2):135–55.

    Article  PubMed  CAS  Google Scholar 

  74. Duda RO, Hart PE, Stork DG. Pattern classification. 2nd ed. New York: Wiley; 2001.

    Google Scholar 

  75. Simen P, Balci F, de Souza L, Cohen JD, Holmes P. A model of interval timing by neural integration. J Neurosci. 2011;31(25):9238–53. Epub 2011/06/24.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  76. Durstewitz D. Neural representation of interval time. Neuroreport. 2004;15(5):745–9.

    Article  PubMed  Google Scholar 

  77. Fuster JM. The prefrontal cortex : anatomy, physiology, and neuropsychology of the frontal lobe. 3rd ed. Philadelphia: Lippincott-Raven; 1997. xvi, 333 p.

    Google Scholar 

  78. Swanton DN, Gooch CM, Matell MS. Averaging of temporal memories by rats. J Exp Psychol Anim Behav Process. 2009;35(3):434–9. Epub 2009/07/15.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Kurti A, Swanton DN, Matell MS. The potential link between temporal averaging and drug-taking behavior. In: Arstila V, Lloyd D, editors. Subjective time. Cambridge: MIT Press; 2014. p. 599–620.

    Google Scholar 

  80. Swanton DN, Matell MS. Stimulus compounding in interval timing: the modality-duration relationship of the anchor durations results in qualitatively different response patterns to the compound cue. J Exp Psychol Anim Behav Process. 2011;37(1):94–107. Epub 2010/08/20.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Matell MS, Kurti AN. Reinforcement probability modulates temporal memory selection and integration processes. Acta Psychol (Amst). 2013. Epub 2013/07/31.

    Google Scholar 

  82. Staddon JER, Higa JJ. Time and memory: towards a pacemaker-free theory of interval timing. J Exp Anal Behav. 1999;71(2):215–51.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  83. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 2000;4(6):215–22. Epub 2000/05/29.

    Article  PubMed  Google Scholar 

  84. Shuler MG, Bear MF. Reward timing in the primary visual cortex. Science. 2006;311(5767):1606–9.

    Article  PubMed  CAS  Google Scholar 

  85. Schneider BA, Ghose GM. Temporal production signals in parietal cortex. PLoS Biol. 2012;10(10):e1001413. Epub 2012/11/03.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  86. Shinomoto S, Omi T, Mita A, Mushiake H, Shima K, Matsuzaka Y, et al. Deciphering elapsed time and predicting action timing from neuronal population signals. Front Comput Neurosci. 2011;5:29. Epub 2011/07/08.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Itskov V, Curto C, Pastalkova E, Buzsaki G. Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J Neurosci. 2011;31(8):2828–34. Epub 2011/03/19.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  88. Laje R, Buonomano DV. Robust timing and motor patterns by taming chaos in recurrent neural networks. Nat Neurosci. 2013;16(7):925–33. Epub 2013/05/28.

    Article  PubMed  CAS  Google Scholar 

  89. Johnson HA, Goel A, Buonomano DV. Neural dynamics of in vitro cortical networks reflects experienced temporal patterns. Nat Neurosci. 2010;13(8):917–9. Epub 2010/06/15.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  90. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron. 2011;71(4):737–49. Epub 2011/08/27.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  91. Merchant H, Perez O, Zarco W, Gamez J. Interval tuning in the primate medial premotor cortex as a general timing mechanism. J Neurosci. 2013;33(21):9082–96. Epub 2013/05/24.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Villanova University, Philadelphia, PA, USA

    Matthew S. Matell

Authors
  1. Matthew S. Matell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew S. Matell .

Editor information

Editors and Affiliations

  1. Campus Juriquilla, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Queretaro, Querétaro, Mexico

    Hugo Merchant

  2. Campus Juriquilla, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Queretaro, Querétaro, Mexico

    Victor de Lafuente

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Matell, M.S. (2014). Searching for the Holy Grail: Temporally Informative Firing Patterns in the Rat. In: Merchant, H., de Lafuente, V. (eds) Neurobiology of Interval Timing. Advances in Experimental Medicine and Biology, vol 829. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1782-2_12

Download citation

Publish with us

Policies and ethics

Search

Navigation