Temporal Expectation Indexed by Pupillary Response

In: Timing & Time Perception
View More View Less
  • 1 Columbia University, USA
  • 2 Koç University, Turkey
  • 3 University of Groningen, Netherlands

Purchase instant access (PDF download and unlimited online access):

€25.00$30.00

Forming temporal expectations plays an instrumental role for the optimization of behavior and allocation of attentional resources. Although the effects of temporal expectations on visual attention are well-established, the question of whether temporal predictions modulate the behavioral outputs of the autonomic nervous system such as the pupillary response remains unanswered. Therefore, this study aimed to obtain an online measure of pupil size while human participants were asked to differentiate between visual targets presented after varying time intervals since trial onset. Specifically, we manipulated temporal predictability in the presentation of target stimuli consisting of letters which appeared after either a short or long delay duration (1.5 vs. 3 s) in the majority of trials (75%) within different test blocks. In the remaining trials (25%), no target stimulus was present to investigate the trajectory of preparatory pupillary response under a low level of temporal uncertainty. The results revealed that the rate of preparatory pupillary response was contingent upon the time of target appearance such that pupils dilated at a higher rate when the targets were expected to appear after a shorter as compared to a longer delay period irrespective of target presence. The finding that pupil size can track temporal regularities and exhibit differential preparatory response between different delay conditions points to the existence of a distributed neural network subserving temporal information processing which is crucial for cognitive functioning and goal-directed behavior.

  • Agostino P.V., , & Cheng R.K. (2016). Contributions of dopaminergic signaling to timing accuracy and precision. Curr. Opin. Behav. Sci., 8, 153160.

    • Search Google Scholar
    • Export Citation
  • Anderson B., , & Sheinberg D. (2008). Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex. Neuropsychologia, 46, 947957.

    • Search Google Scholar
    • Export Citation
  • Backs R.W., , & Walrath L.C. (1992). Eye movement and pupillary response indices of mental workload during visual search of symbolic displays. Appl. Ergon., 23, 243254.

    • Search Google Scholar
    • Export Citation
  • Balcı F., , & Simen P. (2016). A decision model of timing. Curr. Opin. Behav. Sci., 8, 94101.

  • Binda P., , Pereverzeva M., , & Murray S.O. (2014). Pupil size reflects the focus of feature-based attention. J. Neurophysiol., 112, 30463052.

    • Search Google Scholar
    • Export Citation
  • Bradshaw J.L. (1968). Pupillary changes and reaction time with varied stimulus uncertainty. Psychon. Sci., 13, 6970.

  • Brainard D.H. (1997). The psychophysics toolbox. Spat. Vis., 10, 433436.

  • Bueti D., , Bahrami B., , Walsh V., , & Rees G. (2010). Encoding of temporal probabilities in the human brain. J. Neurosci., 30, 43434352.

  • Buhusi C.V., , & Meck W.H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nat. Rev. Neurosci., 6, 755765.

    • Search Google Scholar
    • Export Citation
  • Cellini N., , Mioni G., , Levorato I., , Grondin S., , Stablum F., , & Sarlo M. (2015). Heart rate variability helps tracking time more accurately. Brain Cogn., 101, 5763.

    • Search Google Scholar
    • Export Citation
  • Chun M.M., , & Potter M.C., (2001). The attentional blink and task switching within and across modalities. In Shapiro K. (Ed.), The limits of Attention: Temporal Constraints in Human Information Processing (pp. 2035). New York, NY, USA: Oxford University Press.

    • Search Google Scholar
    • Export Citation
  • Cornelissen F.W., , Peters E.M., , & Palmer J. (2002). The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox. Behav. Res. Methods Instrum. Comput., 34, 613617.

    • Search Google Scholar
    • Export Citation
  • Correa Á., , Lupiáñez J., , Milliken B., , & Tudela P. (2004). Endogenous temporal orienting of attention in detection and discrimination tasks. Percept. Psychophys., 66, 264278.

    • Search Google Scholar
    • Export Citation
  • Coull J.T. (2009). Neural substrates of mounting temporal expectation. PLoS Biol., 7, e1000166. doi:10.1371/journal.pbio.1000166 .

  • Coull J.T., , & Nobre A.C. (1998). Where and when to pay attention: The neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. J. Neurosci., 18, 74267435.

    • Search Google Scholar
    • Export Citation
  • Coull J.T., , & Nobre A.C. (2008). Dissociating explicit timing from temporal expectation with fMRI. Curr. Opin. Neurobiol., 18, 137144.

  • Coull J.T., , Nobre A.C., , & Frith C.D. (2001). The noradrenergic α2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting. Cereb. Cortex, 11, 7384.

    • Search Google Scholar
    • Export Citation
  • Coull J.T., , Cheng R.K., , & Meck W.H. (2011). Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology, 36, 325.

  • Cravo A., , Rohenkohl G., , Wyart V., , & Nobre A. (2013). Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex. J. Neurosci., 33, 40024010.

    • Search Google Scholar
    • Export Citation
  • Cui X., , Stetson C., , Montague P.R., , & Eagleman D.M. (2009). Ready… Go: Amplitude of the fMRI signal encodes expectation of cue arrival time. PLoS Biol., 7, e1000167. doi:10.1371/journal.pbio.1000167 .

    • Search Google Scholar
    • Export Citation
  • Finnerty G.T., , Shadlen M.N., , Jazayeri M., , Nobre A.C., , & Buonomano D.V. (2015). Time in cortical circuits. J. Neurosci., 35, 1391213916.

  • Ghose G., , & Maunsell J. (2002). Attentional modulation in visual cortex depends on task timing. Nature, 419(6907), 616620. doi:10.1038/nature01057 .

    • Search Google Scholar
    • Export Citation
  • Gilzenrat M.S., , Nieuwenhuis S., , Jepma M., , & Cohen J.D. (2010). Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn. Affect. Behav. Neurosci., 10, 252269.

    • Search Google Scholar
    • Export Citation
  • Henry M.J., , & Hermann B. (2014). Low-frequency neural oscillations support dynamic attending in temporal context. Timing Time Percept., 2, 6286.

    • Search Google Scholar
    • Export Citation
  • Hoeks B., , & Levelt W.J. (1993). Pupillary dilation as a measure of attention: A quantitative system analysis. Behav. Res. Methods Instrum. Comput., 25, 1626.

    • Search Google Scholar
    • Export Citation
  • Hoppe D., , & Rothkopf C.A. (2016). Learning rational temporal eye movement strategies. Proc. Natl Acad. Sci. USA, 113, 83328337.

  • Hupé J.M., , Lamirel C., , & Lorenceau J. (2009). Pupil dynamics during bistable motion perception. J. Vis., 9, 10. doi: 10.1167/9.7.10 .

  • Jainta S., , Vernet M., , Yang Q., , & Kapoula Z. (2011). The pupil reflects motor preparation for saccades—Even before the eye starts to move. Front. Hum. Neurosci., 5, 97. doi: 10.3389/fnhum.2011.00097 .

    • Search Google Scholar
    • Export Citation
  • Janssen P., , & Shadlen M.N. (2005). A representation of the hazard rate of elapsed time in macaque area LIP. Nat. Neurosci., 8, 234241.

  • Jennings J.R., , Molen M.W., , & Steinhauer S.R. (1998). Preparing the heart, eye, and brain: Foreperiod length effects in a nonaging paradigm. Psychophysiology, 35, 9098.

    • Search Google Scholar
    • Export Citation
  • Kang O.E., , Huffer K.E., , & Wheatley T.P. (2014). Pupil dilation dynamics track attention to high-level information. PloS One, 9, e102463. doi: 10.1371/journal.pone.0102463 .

    • Search Google Scholar
    • Export Citation
  • Karşılar H., , & Balcı F. (in press). Asymmetrical modulation of time perception by increase versus decrease in coherence of motion. Atten. Percept. Psychophys. doi: 10.3758/s13414-016-1181-9 .

    • Search Google Scholar
    • Export Citation
  • Kinsbourne M., , & Warrington E.K. (1962). The effect of an after-coming random pattern on the perception of brief visual stimuli. Q.J. Exp. Psychol., 14, 223234.

    • Search Google Scholar
    • Export Citation
  • Knapen T., , De Gee J.W., , Brascamp J., , Nuiten S., , Hoppenbrouwers S., , & Theeuwes J. (2016). Cognitive and ocular factors jointly determine pupil responses under equiluminance. PLoS OneE, 11, e0155574. doi: 10.1371/journal.pone.0155574 .

    • Search Google Scholar
    • Export Citation
  • Kononowicz T.W., , & Penney T.B. (2016). The contingent negative variation (CNV): Timing isn’t everything. Curr. Opin. Behav. Sci., 8, 231237.

    • Search Google Scholar
    • Export Citation
  • Kononowicz T.W., , & Van Rijn H. (2011). Slow potentials in time estimation: The role of temporal accumulation and habituation. Front. Integ. Neurosci., 5, 48. doi: 10.3389/fnint.2011.00048 .

    • Search Google Scholar
    • Export Citation
  • Kononowicz T.W., , Van Rijn H., , & Meck W.H., (in press). Timing and time perception: A critical review of neural timing signatures before, during, and after the to-be-timed interval. In Wixted J., (Editor-in-Chief) and Serences J. (Ed., Vol. II), Sensation, Perception and Attention, Volume II – Stevens’ Handbook of Experimental Psychology and Cognitive Neuroscience (4th ed.) (pp. 135). New York, NY, USA: Wiley.

    • Search Google Scholar
    • Export Citation
  • Laeng B., , Sirois S., , & Gredebäck G. (2012). Pupillometry: A window to the preconscious? Perspect. Psychol. Sci., 7, 1827.

  • Lima B., , Singer W., , & Neuenschwander S. (2011). Gamma responses correlate with temporal expectation in monkey primary visual cortex. J. Neurosci., 31, 1591915931.

    • Search Google Scholar
    • Export Citation
  • Lusk N.A., , Petter E.A., , MacDonald C.J., , & Meck W.H. (2016). Cerebellar, hippocampal, and striatal time cells. Curr. Opin. Behav. Sci., 8, 186191.

    • Search Google Scholar
    • Export Citation
  • Macar F., , & Vidal F. (2009). Timing processes: An outline of behavioural and neural indices not systematically considered in timing models. Can. J. Exp. Psychol., 63, 227239.

    • Search Google Scholar
    • Export Citation
  • Matthews W.J., , & Meck W.H. (2016). Temporal cognition: Connecting subjective duration to perception, attention, and memory. Psychol. Bull., 142, 865907.

    • Search Google Scholar
    • Export Citation
  • Meissner K., , & Wittmann M. (2011). Body signals, cardiac awareness, and the perception of time. Biol. Psychol., 86, 289297.

  • Moresi S., , Adam J.J., , Rijcken J., , Van Gerven P.W., , Kuipers H., , & Jolles J. (2008). Pupil dilation in response preparation. Int. J. Psychophysiol., 67, 124130.

    • Search Google Scholar
    • Export Citation
  • Mueller S.T., , & Weidemann C.T. (2012). Alphabetic letter identification: Effects of perceivability, similarity, and bias. Acta Psychol., 139, 1937.

    • Search Google Scholar
    • Export Citation
  • Naber M., , Frässle S., , Rutishauser U., , & Einhäuser W. (2013). Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes. J. Vis., 13, 11. doi: 10.1167/13.2.11 .

    • Search Google Scholar
    • Export Citation
  • Niemi P., , & Näätänen R. (1981). Foreperiod and simple reaction time. Psychol. Bull., 89, 133162.

  • Namboodiri V.M.K., , Huertas M.A., , Monk K.J., , Shouval H.Z., , & Shuler M.G.H. (2015). Visually cued action timing in the primary visual cortex. Neuron, 86, 319330.

    • Search Google Scholar
    • Export Citation
  • Nobre A., , Correa A., , & Coull J. (2007). The hazards of time. Curr. Opin. Neurobiol., 17, 465470.

  • Pelli D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spat. Vis., 10, 437442.

  • Penney T.B., , Cheng X., , Leow Y.L., , Bay A.W.Y., , Wu E.W., , Herbst S.K., , & Yen S.C. (2016). Saccades and subjective time in seconds range duration reproduction. Timing Time Percept. , 4, 187206.

    • Search Google Scholar
    • Export Citation
  • Pfeuty M., , Ragot R., , & Pouthas V. (2005). Relationship between CNV and timing of an upcoming event. Neurosci. Lett., 382, 106111.

  • Pinheiro J.C., , & Bates D.M. (2000). Mixed-effects models in S and S-PLUS. New York, NY, USA: Springer Verlag.

  • Pollatos O., , Yeldesbay A., , Pikovsky A., , & Rosenblum M. (2014). How much time has passed? Ask your heart. Front. Neurorobot., 8, 15. doi: 10.3389/fnbot.2014.00015 .

    • Search Google Scholar
    • Export Citation
  • Raisig S., , Welke T., , Hagendorf H., , & Van der Meer E. (2010). I spy with my little eye: Detection of temporal violations in event sequences and the pupillary response. Int. J. Psychophysiol., 76, 18.

    • Search Google Scholar
    • Export Citation
  • Reuter-Lorenz P., , Oonk H., , Barnes L., , & Hughes H. (1995). Effects of warning signals and fixation point offsets on the latencies of pro- versus antisaccades: Implications for an interpretation of the gap effect. Exp. Brain Res., 103, 287293.

    • Search Google Scholar
    • Export Citation
  • Richer F., , & Beatty J. (1985). Pupillary dilations in movement preparation and execution. Psychophysiology, 22, 204207.

  • Rivest F., , & Bengio Y. (2011). Adaptive drift-diffusion process to learn time intervals. arXiv:1103.2382v1.

  • Rolke B., , & Ulrich R., (2010). On the locus of temporal preparation: Enhancement of premotor processes. In Nobre A.C., & Coull J.T. (Eds), Attention and Time (pp. 227242). Oxford, UK: Oxford University Press.

    • Search Google Scholar
    • Export Citation
  • Schirmer A., , Meck W.H., , & Penney T.B. (2016). The socio-temporal brain: Connecting people in time. Trends Cogn. Sci., 20(10), 760772.

  • Schultz W. (1998). Predictive reward signal of dopamine neurons. J. Neurophysiol., 80, 127.

  • Schultz W., , Dayan P., , & Montague P.R. (1997). A neural substrate of prediction and reward. Science, 275, 15931599.

  • Schütz A.C., , & Morrone M.C. (2010). Compression of time during smooth pursuit eye movements. Vis. Res., 50(24), 27022713.

  • Shuler M., , & Bear M. (2006). Reward timing in the primary visual cortex. Science , 311, 16061609.

  • Simen P., , Balcı F., , deSouza L., , Cohen J.D., , & Holmes P. (2011). A model of interval timing by neural integration. J. Neurosci., 31, 92389253.

    • Search Google Scholar
    • Export Citation
  • Taylor J.R., , Elsworth J.D., , Lawrence M.S., , Sladek J.R., , Roth R.H., , & Redmond D.E. (1999). Spontaneous blink rates correlate with dopamine levels in the caudate nucleus of MPTP-treated monkeys. Exp. Neurol., 158, 214220.

    • Search Google Scholar
    • Export Citation
  • Terhune D.B., , Sullivan J.G., , & Simola J.M., (2016). Time dilates after spontaneous blinking. Curr. Biol ., 26, R59R60.Thomaschke R., , Wagener A., , Kiesel A., , & Hoffmann J. (2011). The scope and precision of specific temporal expectancy: Evidence from a variable foreperiod paradigm. Atten. Percept. Psychophys., 73, 953964.

    • Search Google Scholar
    • Export Citation
  • Thomaschke R., , Hoffmann J., , Haering C., , & Kiesel A. (in press). Time-based expectancy for task relevant stimulus features. Timing Time Percept. doi: 10.1163/22134468-00002069 .

    • Search Google Scholar
    • Export Citation
  • Toscano-Zapién A.L., , Velázquez-López D., , & Velázquez-Martínez D.N. (2016). Attentional mechanisms during the performance of a subsecond timing task. PloS One, 11, e0158508. doi: 10.1371/journal.pone.0158508 .

    • Search Google Scholar
    • Export Citation
  • Tressoldi P.E., , Martinelli M., , Semenzato L., , & Cappato S. (2011). Let your eyes predict: Prediction accuracy of pupillary responses to random alerting and neutral sounds. Sage Open, 17. doi: 10.1177/2158244011420451 .

    • Search Google Scholar
    • Export Citation
  • Van Orden K.F., , Limbert W., , Makeig S., , & Jung T.P. (2001). Eye activity correlates of workload during a visuospatial memory task. Hum. Factors, 43, 111121.

    • Search Google Scholar
    • Export Citation
  • Van Rijn H., , Kononowicz T.W., , Meck W.H., , Ng K.K., , & Penney T.B. (2011). Contingent negative variation and its relation to time estimation: A theoretical evaluation. Front. Int. Neurosci.. 5, 91. doi: 10.3389/fnint.2011.00091 .

    • Search Google Scholar
    • Export Citation
  • Van Rijn H., , Dalenberg J.R., , Borst J.P., , & Sprenger S.A. (2012). Pupil dilation co-varies with memory strength of individual traces in a delayed response paired-associate task. PLoS One, 7, e51134. doi: 10.1371/journal.pone.0051134 .

    • Search Google Scholar
    • Export Citation
  • Vangkilde S., , Petersen A., , & Bundesen C. (2013). Temporal expectancy in the context of a theory of visual attention. Phil. Trans. R. Soc. B. Biol. Sci., 368(1628), 20130054. doi: 10.1098/rtsb.2013.0054 .

    • Search Google Scholar
    • Export Citation
  • Wierda S., , Van Rijn H., , Taatgen N., , & Martens S. (2012). Pupil dilation deconvolution reveals the dynamics of attention at high temporal resolution. Proc. Natl Acad. Sci. USA, 109, 84568460.

    • Search Google Scholar
    • Export Citation
  • Willems C., , Damsma A., , Wierda S.M., , Taatgen N., , & Martens S. (2015). Training-induced changes in the dynamics of attention as reflected in pupil dilation. J. Cogn. Neurosci., 27, 11611171.

    • Search Google Scholar
    • Export Citation
  • Wittmann M. (2013). The inner sense of time: How the brain creates a representation of duration. Nat. Rev. Neurosci., 14, 217223.

  • Witte E.A., , & Marrocco R.T. (1997). Alteration of brain noradrenergic activity in rhesus monkeys affects the alerting component of covert orienting. Psychopharmacology, 132, 315323.

    • Search Google Scholar
    • Export Citation
  • Yamamoto K.I., , & Ozawa N. (1989). Increased firing of locus coeruleus neurons associated with preparatory set in rats. Neurosci. Lett., 106, 112118.

    • Search Google Scholar
    • Export Citation
  • Zylberberg A., , Oliva M., , & Sigman M. (2012). Pupil dilation: A fingerprint of temporal selection during the “attentional blink”. Front. Psychol., 3, 316. doi: 10.3389/fpsyg.2012.00316 .

    • Search Google Scholar
    • Export Citation

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 380 195 13
Full Text Views 261 19 3
PDF Downloads 54 15 1