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Anticipation of future events improves the ability to estimate elapsed time

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Abstract

An accurate estimate of elapsed time is essential for anticipating the timing of future events. Here, we show that the ability to estimate elapsed time on a reaction time (RT) task improved with training during which human participants learned to anticipate the onset of a “Go” signal. In each trial, a warning signal preceded the Go signal by a temporal interval (i.e., foreperiod). The duration of the foreperiod was randomly drawn from a rectangular distribution (1–2 s). Participants were required to initiate a response immediately after the Go signal and performed the task for 480 trials/day for 12 days. Anticipation should have been governed by the probability that the Go signal would occur (hazard rate), which increased for longer foreperiods. Indeed, RTs decreased for longer foreperiods and were inversely related to the hazard rate. The pattern of RT decrease was well explained by the subjective hazard rate, which was formalized based on the assumption that the uncertainty of estimates of elapsed time scales with time (Weber’s law). Notably, RTs demonstrated a more linear decrease as a function of foreperiod in LATE compared with EARLY training sessions. This involved a decrease in the Weber fraction used in the subjective hazard rate. The results indicate that the uncertainty associated with estimating elapsed time was reduced as participants learned and used the hazard rate to anticipate the onset of the Go signal. This finding suggests that the ability to estimate elapsed time improves with training on behavioral tasks that implicitly engage timing mechanisms.

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References

  • Bartolo R, Merchant H (2009) Learning and generalization of time production in humans: rules of transfer across modalities and interval durations. Exp Brain Res 197:91–100

    Article  PubMed  Google Scholar 

  • Brody CD, Hernandez A, Zainos A, Romo R (2003) Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb Cortex 13:1196–1207

    Article  PubMed  Google Scholar 

  • Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci 6:755–765

    Article  PubMed  CAS  Google Scholar 

  • Coull JT, Nobre AC (2008) Dissociating explicit timing from temporal expectation with fMRI. Curr Opin Neurobiol 18:137–144

    Article  PubMed  CAS  Google Scholar 

  • Cui X, Stetson C, Montague PR, Eagleman DM (2009) Ready…go: amplitude of the fMRI signal encodes expectation of cue arrival time. PLoS Biol 7:e1000167

    Article  PubMed  Google Scholar 

  • Drazin DH (1961) Effects of foreperiod, foreperiod variability, and probability of stimulus occurrence on simple reaction time. J Exp Psychol 62:43–50

    Article  PubMed  CAS  Google Scholar 

  • Durstewitz D (2003) Self-organizing neural integrator predicts interval times through climbing activity. J Neurosci 23:5342–5353

    PubMed  CAS  Google Scholar 

  • Eagleman DM, Tse PU, Buonomano D, Janssen P, Nobre AC, Holcombe AO (2005) Time and the brain: how subjective time relates to neural time. J Neurosci 25:10369–10371

    Article  PubMed  CAS  Google Scholar 

  • Elithorn A, Lawrence C (1955) Central inhibition—some refractory observations. Q J Exp Psychol 7:116–127

    Article  Google Scholar 

  • Fischer B, Rogal L (1986) Eye-hand-coordination in man: a reaction time study. Biol Cybern 55:253–261

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gibbon J, Malapani C, Dale CL, Gallistel C (1997) Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol 7:170–184

    Article  PubMed  CAS  Google Scholar 

  • Gorbet DJ, Sergio LE (2009) The behavioural consequences of dissociating the spatial directions of eye and arm movements. Brain Res 1284:77–88

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DS, Strick PL (1986) Step-tracking movements of the wrist in humans. I. Kinematic analysis. J Neurosci 6:3309–3318

    PubMed  CAS  Google Scholar 

  • Hoffman DS, Strick PL (1999) Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. J Neurophysiol 81:319–333

    PubMed  CAS  Google Scholar 

  • Ivry RB (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6:851–857

    Article  PubMed  CAS  Google Scholar 

  • Janssen P, Shadlen MN (2005) A representation of the hazard rate of elapsed time in macaque area LIP. Nat Neurosci 8:234–241

    Article  PubMed  CAS  Google Scholar 

  • Kakei S, Hoffman DS, Strick PL (1999) Muscle and movement representations in the primary motor cortex. Science 285:2136–2139

    Article  PubMed  CAS  Google Scholar 

  • Karlin L (1959) Reaction time as function of foreperiod duration and variability. J Exp Psychol 58:185–191

    Article  PubMed  CAS  Google Scholar 

  • Karmarkar UR, Buonomano DV (2003) Temporal specificity of perceptual learning in an auditory discrimination task. Learn Mem 10:141–147

    Article  PubMed  Google Scholar 

  • Klemmer ET (1956) Time uncertainty in simple reaction time. J Exp Psychol 51:179–184

    Article  PubMed  CAS  Google Scholar 

  • Komura Y, Tamura R, Uwano T, Nishijo H, Kaga K, Ono T (2001) Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature 412:546–549

    Article  PubMed  CAS  Google Scholar 

  • Leon MI, Shadlen MN (2003) Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38:317–327

    Article  PubMed  CAS  Google Scholar 

  • Lewis PA, Miall RC (2003) Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol 13:250–255

    Article  PubMed  CAS  Google Scholar 

  • Loveless NE (1973) The contingent negative variation related to preparatory set in a reaction time situation with variable foreperiod. Electroencephalogr Clin Neurophysiol 35:369–374

    Article  PubMed  CAS  Google Scholar 

  • Luce RD (1986) Response times: their role in inferring elementary mental organization. Oxford University Press, New York

    Google Scholar 

  • Macar F, Vidal F, Casini L (1999) The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes. Exp Brain Res 125:271–280

    Article  PubMed  CAS  Google Scholar 

  • MacDonald CJ, Meck WH (2006) Interaction of raclopride and preparatory interval effects on simple reaction time performance. Behav Brain Res 175:62–74

    Article  PubMed  CAS  Google Scholar 

  • Mauk MD, Buonomano DV (2004) The neural basis of temporal processing. Annu Rev Neurosci 27:307–340

    Article  PubMed  CAS  Google Scholar 

  • Mauritz KH, Wise SP (1986) Premotor cortex of the rhesus monkey: neuronal activity in anticipation of predictable environmental events. Exp Brain Res 61:229–244

    Article  PubMed  CAS  Google Scholar 

  • Meegan DV, Aslin RN, Jacobs RA (2000) Motor timing learned without motor training. Nat Neurosci 3:860–862

    Article  PubMed  CAS  Google Scholar 

  • Merchant H, Zarco W, Bartolo R, Prado L (2008) The context of temporal processing is represented in the multidimensional relationships between timing tasks. PLoS One 3:e3169

    Article  PubMed  Google Scholar 

  • Mita A, Mushiake H, Shima K, Matsuzaka Y, Tanji J (2009) Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat Neurosci 12:502–507

    Article  PubMed  CAS  Google Scholar 

  • Näätänen R, Merisalo A (1977) Expectancy and preparation in simple reaction time. In: Dornic S (ed) Attention and performance VI. Lawrence Erlbaum, Hillsdale, pp 115–138

    Google Scholar 

  • Nagarajan SS, Blake DT, Wright BA, Byl N, Merzenich MM (1998) Practice-related improvements in somatosensory interval discrimination are temporally specific but generalize across skin location, hemisphere, and modality. J Neurosci 18:1559–1570

    PubMed  CAS  Google Scholar 

  • Niemi P, Näätänen R (1981) Foreperiod and simple reaction time. Psychol Bull 89:133–162

    Article  Google Scholar 

  • Niki H, Watanabe M (1979) Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res 171:213–224

    Article  PubMed  CAS  Google Scholar 

  • Nobre AC, Correa A, Coull JT (2007) The hazards of time. Curr Opin Neurobiol 17:465–470

    Article  PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Oswal A, Ogden M, Carpenter RHS (2007) The time course of stimulus expectation in a saccadic decision task. J Neurophysiol 97:2722–2730

    Article  PubMed  CAS  Google Scholar 

  • Polzella DJ, Ramsey EG, Bower SM (1989) The effects of brief variable foreperiods on simple reaction time. Bull Psychon Soc 27:467–469

    Google Scholar 

  • Praamstra P, Kourtis D, Kwok HF, Oostenveld R (2006) Neurophysiology of implicit timing in serial choice reaction-time performance. J Neurosci 26:5448–5455

    Article  PubMed  CAS  Google Scholar 

  • Requin J, Granjon M (1969) The effect of conditional probability of the response signal on the simple reaction time. Acta Psychol (Amst) 31:129–144

    Article  CAS  Google Scholar 

  • Reutimann J, Yakovlev V, Fusi S, Senn W (2004) Climbing neuronal activity as an event-based cortical representation of time. J Neurosci 24:3295–3303

    Article  PubMed  CAS  Google Scholar 

  • Riehle A, Grun S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950–1953

    Article  PubMed  CAS  Google Scholar 

  • Rosenbaum DA (1980) Human movement initiation: specification of arm, direction, and extent. J Exp Psychol Gen 109:444–474

    Article  PubMed  CAS  Google Scholar 

  • Ruchkin DS, McCalley MG, Glaser EM (1977) Event related potentials and time estimation. Psychophysiology 14:451–455

    Article  PubMed  CAS  Google Scholar 

  • Trillenberg P, Verleger R, Wascher E, Wauschkuhn B, Wessel K (2000) CNV and temporal uncertainty with ‘ageing’ and ‘non-ageing’ S1–S2 intervals. Clin Neurophysiol 111:1216–1226

    Article  PubMed  CAS  Google Scholar 

  • Tsunoda Y, Kakei S (2008) Reaction time changes with the hazard rate for a behaviorally relevant event when monkeys perform a delayed wrist movement task. Neurosci Lett 433:152–157

    Article  PubMed  CAS  Google Scholar 

  • Walter WG, Cooper R, Aldridge VJ, Mccallum WC, Winter AL (1964) Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 203:380–384

    Article  PubMed  CAS  Google Scholar 

  • Westheimer G (1999) Discrimination of short time intervals by the human observer. Exp Brain Res 129:121–126

    Article  PubMed  CAS  Google Scholar 

  • Wright BA, Buonomano DV, Mahncke HW, Merzenich MM (1997) Learning and generalization of auditory temporal-interval discrimination in humans. J Neurosci 17:3956–3963

    PubMed  CAS  Google Scholar 

  • Yamamoto K, Hoffman DS, Strick PL (2006) Rapid and long-lasting plasticity of input-output mapping. J Neurophysiol 96:2797–2801

    Article  PubMed  Google Scholar 

  • Zelaznik HN, Spencer RM, Ivry RB (2002) Dissociation of explicit and implicit timing in repetitive tapping and drawing movements. J Exp Psychol Hum Percept Perform 28:575–588

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Drs. Jongho Lee and Saeka Tomatsu for valuable comments. We are also grateful to Drs. Michael Shadlen, Masaaki Doi, Akitoshi Ogawa, Tung Le, and Nobuto Takeuchi for thoughtful discussions. This work was supported by KAKENHI (#16015212 to SK).

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Correspondence to Yoshiaki Tsunoda.

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Tsunoda, Y., Kakei, S. Anticipation of future events improves the ability to estimate elapsed time. Exp Brain Res 214, 323–334 (2011). https://doi.org/10.1007/s00221-011-2821-x

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