Abstract
The term ‘timing’ is interchangeably used to convey processing of the order or the duration of events. Yet, whereas temporal order processing means judging when one event happens relative to another (first or second), duration estimation means measuring how long the event lasts. In this Review, we show that the functional distinction between these two temporal features is reflected in their discrete neural substrates. Temporal order processing preferentially engages the left inferior parietal cortex, whereas duration estimation recruits the supplementary motor area, basal ganglia and cerebellum. The functional distinction between temporal order processing and duration estimation also enables better characterization of temporal perturbations present in clinical disorders. For instance, individuals with schizophrenia have trouble individuating and ordering consecutive events in time and show atypical responses to stimuli that do not appear when expected. Therefore, individuals with schizophrenia might have a fundamental impairment in processing when a stimulus occurs relative to another event, rather than in estimating how long it lasts. These neural and clinical dissociations demonstrate that the phenomenological sensation of a unitary and cohesive flow of time (‘time’s arrow’) can be separated into two distinct, though intertwined, components.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 digital issues and online access to articles
$59.00 per year
only $4.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Van Heuven, W. J. B., Mandera, P., Keuleers, E. & Brysbaert, M. Subtlex-UK: a new and improved word frequency database for British English. Q. J. Exp. Psychol. 67, 1176–1190 (2014).
Winter, B., Marghetis, T. & Matlock, T. Of magnitudes and metaphors: explaining cognitive interactions between space, time, and number. Cortex 64, 209–224 (2015).
Boroditsky, L. Language and the construction of time through space. Trends Neurosci. 41, 651–653 (2018).
Fraisse, P. Perception and estimation of time. Annu. Rev. Psychol. 35, 1–36 (1984).
Block, R. A. (ed.) in Cognitive Models Of Psychological Time 1–36 (Erlbaum, 1990).
Pöppel, E. A hierarchical model of temporal perception. Trends Cogn. Sci. 1, 56–61 (1997).
Teki, S. A citation-based analysis and review of significant papers on timing and time perception. Front. Neurosci. 10, 330 (2016).
Wittmann, M. Time perception and temporal processing levels of the brain. Chronobiol. Int. 16, 17–32 (1999).
van Wassenhove, V. Minding time in an amodal representational space. Phil. Trans. R. Soc. B 364, 1815–1830 (2009).
Grondin, S. Timing and time perception: a review of recent behavioral and neuroscience findings and theoretical directions. Atten. Percept. Psychophys. 72, 561–582 (2010).
Coull, J. T. & Nobre, A. Dissociating explicit timing from temporal expectation with fMRI. Curr. Opin. Neurobiol. 18, 137–144 (2008).
Paton, J. J. & Buonomano, D. V. The neural basis of timing: distributed mechanisms for diverse functions. Neuron 98, 687–705 (2018).
Thönes, S. & Stocker, K. A standard conceptual framework for the study of subjective time. Conscious. Cogn. 71, 114–122 (2019).
Thoenes, S. & Oberfeld, D. Meta-analysis of time perception and temporal processing in schizophrenia: differential effects on precision and accuracy. Clin. Psychol. Rev. 54, 44–64 (2017).
Vatakis, A., Navarra, J., Soto-Faraco, S. & Spence, C. Audiovisual temporal adaptation of speech: temporal order versus simultaneity judgments. Exp. Brain Res. 185, 521–529 (2008).
Love, S. A., Petrini, K., Cheng, A. & Pollick, F. E. A psychophysical investigation of differences between synchrony and temporal order judgments. PLoS ONE 8, e54798 (2013).
García-Pérez, M. A. & Alcalá-Quintana, R. Converging evidence that common timing processes underlie temporal-order and simultaneity judgments: a model-based analysis. Atten. Percept. Psychophys. 77, 1750–1766 (2015).
Binder, M. Neural correlates of audiovisual temporal processing — comparison of temporal order and simultaneity judgments. Neuroscience 300, 432–447 (2015).
Miyazaki, M. et al. Dissociating the neural correlates of tactile temporal order and simultaneity judgements. Sci. Rep. 6, 23323 (2016).
Recio, R. S., Cravo, A. M., de Camargo, R. Y. & van Wassenhove, V. Dissociating the sequential dependency of subjective temporal order from subjective simultaneity. PLoS ONE 14, e0223184 (2019).
Marshuetz, C. Order information in working memory: an integrative review of evidence from brain and behavior. Psychol. Bull. 131, 323–339 (2005).
Davachi, L. & DuBrow, S. How the hippocampus preserves order: the role of prediction and context. Trends Cogn. Sci. 19, 92–99 (2015).
Kostaki, M. & Vatakis, A. Tin Timing And Time Perception: Procedures, Measures And Application (eds Vatakis, A., Balci, F., Di Luca, M. & Correa, A.) 233–262 (Brill, 2018).
Machulla, T. K., Di Luca, M. & Ernst, M. O. The consistency of crossmodal synchrony perception across the visual, auditory, and tactile senses. J. Exp. Psychol. Hum. Percept. Perform. 42, 1026–1038 (2016).
van Wassenhove, V., Grant, K. W. & Poeppel, D. Temporal window of integration in auditory-visual speech perception. Neuropsychologia 45, 598–607 (2007).
Hirsh, I. J. & Sherrick, C. E. Jr. Perceived order in different sense modalities. J. Exp. Psychol. 62, 423–432 (1961).
Kanabus, M., Szelag, E., Rojek, E. & Pöppel, E. Temporal order judgement for auditory and visual stimuli. Acta Neurobiol. Exp. 62, 263–270 (2002).
Fink, M., Ulbrich, P., Churan, J. & Wittmann, M. Stimulus-dependent processing of temporal order. Behav. Process. 71, 344–352 (2006).
Herzog, M. H., Kammer, T. & Scharnowski, F. Time slices: what is the duration of a percept? PLoS Biol. 14, e1002433 (2016).
Vatakis, A. & Spence, C. Audiovisual synchrony perception for music, speech, and object actions. Brain Res. 1111, 134–142 (2006).
Stevenson, R. A. & Wallace, M. T. Multisensory temporal integration: task and stimulus dependencies. Exp. Brain Res. 227, 249–261 (2013).
Spence, C. in Attention and Time (eds Nobre, A. C. & Coull, J. T.) 89–104 (Oxford Univ. Press, 2010).
Neumann, O. Direct parameter specification and the concept of perception. Psychol. Res. 52, 207–215 (1990).
Lalanne, L., Van Assche, M., Wang, W. & Giersch, A. Looking forward: an impaired ability in patients with schizophrenia? Neuropsychologia 50, 2736–2744 (2012).
Lalanne, L., van Assche, M. & Giersch, A. When predictive mechanisms go wrong: disordered visual synchrony thresholds in schizophrenia. Schizophr. Bull. 38, 506–513 (2012).
Grabot, L. & van Wassenhove, V. Time order as psychological bias. Psychol. Sci. 28, 670–678 (2017).
Paraskevoudi, N. & Vatakis, A. in The Illusions of Time (eds Arstila, V., Bardon, A., Power, S. E. & Vatakis, A.) 225–257 (Palgrave Macmillan, 2019).
VanRullen, R. Perceptual cycles. Trends Cogn. Sci. 20, 723–735 (2016).
Grabot, L., Kösem, A., Azizi, L. & van Wassenhove, V. Prestimulus alpha oscillations and the temporal sequencing of audiovisual events. J. Cogn. Neurosci. 29, 1566–1582 (2017).
Cecere, R., Rees, G. & Romei, V. Individual differences in alpha frequency drive crossmodal illusory perception. Curr. Biol. 25, 231–235 (2015).
Samaha, J. & Postle, B. R. The speed of alpha-band oscillations predicts the temporal resolution of visual perception. Curr. Biol. 25, 2985–2990 (2015).
Wutz, A., Melcher, D. & Samaha, J. Frequency modulation of neural oscillations according to visual task demands. Proc. Natl Acad. Sci. USA 115, 1346–1351 (2018).
Fiebelkorn, I. C., Saalmann, Y. B. & Kastner, S. Rhythmic sampling within and between objects despite sustained attention at a cued location. Curr. Biol. 23, 2553–2558 (2013).
Helfrich, R. F. et al. Neural mechanisms of sustained attention are rhythmic. Neuron 99, 854–865.e5 (2018).
Davis, B., Christie, J. & Rorden, C. Temporal order judgments activate temporal parietal junction. J. Neurosci. 29, 3182–3188 (2009).
Love, S. A., Petrini, K., Pernet, C. R., Latinus, M. & Pollick, F. E. Overlapping but divergent neural correlates underpinning audiovisual synchrony and temporal order judgments. Front. Hum. Neurosci. 12, 274 (2018).
Moser, D., Baker, J. M., Sanchez, C. E., Rorden, C. & Fridriksson, J. Temporal order processing of syllables in the left parietal lobe. J. Neurosci. 29, 12568–12573 (2009).
Efron, R. The effect of handedness on the perception of simultaneity and temporal order. Brain 86, 261–284 (1963).
Swisher, L. & Hirsh, I. J. Brain damage and the ordering of two temporally successive stimuli. Neuropsychologia 10, 137–152 (1972).
von Steinbüchel, N., Wittmann, M., Strasburger, H. & Szelag, E. Auditory temporal-order judgement is impaired in patients with cortical lesions in posterior regions of the left hemisphere. Neurosci. Lett. 264, 168–171 (1999).
Wencil, E. B., Radoeva, P. & Chatterjee, A. Size isn’t all that matters: noticing differences in size and temporal order. Front. Hum. Neurosci. 4, 171 (2010).
Wittmann, M., Burtscher, A., Fries, W. & von Steinbüchel, N. Effects of brain-lesion size and location on temporal-order judgment. Neuroreport 15, 2401–2405 (2004).
Adhikari, B. M., Goshorn, E. S., Lamichhane, B. & Dhamala, M. Temporal-order judgment of audiovisual events involves network activity between parietal and prefrontal cortices. Brain Connect. 3, 536–545 (2013).
Takahashi, T., Kansaku, K., Wada, M., Shibuya, S. & Kitazawa, S. Neural correlates of tactile temporal-order judgment in humans: an fMRI study. Cereb. Cortex 23, 1952–1964 (2013).
Otsuru, N. et al. 10Hz transcranial alternating current stimulation over posterior parietal cortex facilitates tactile temporal order judgment. Behav. Brain Res. 368, 111899 (2019).
Battelli, L., Pascual-Leone, A. & Cavanagh, P. The ‘when’ pathway of the right parietal lobe. Trends Cogn. Sci. 11, 204–210 (2007).
Woo, S. H., Kim, K. H. & Lee, K. M. The role of the right posterior parietal cortex in temporal order judgment. Brain Cogn. 69, 337–343 (2009).
Tyler, S. C., Contò, F. & Battelli, L. Rapid improvement on a temporal attention task within a single session of high-frequency transcranial random noise stimulation. J. Cogn. Neurosci. 30, 656–666 (2018).
Rorden, C., Mattingley, J. B., Karnath, H. O. & Driver, J. Visual extinction and prior entry: impaired perception of temporal order with intact motion perception after unilateral parietal damage. Neuropsychologia 35, 421–433 (1997).
Robertson, I. H., Mattingley, J. B., Rorden, C. & Driver, J. Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature 395, 169–172 (1998).
Baylis, G. C., Simon, S. L., Baylis, L. L. & Rorden, C. Visual extinction with double simultaneous stimulation: what is simultaneous? Neuropsychologia 40, 1027–1034 (2002).
Agosta, S. et al. The pivotal role of the right parietal lobe in temporal attention. J. Cogn. Neurosci. 29, 805–815 (2017).
Roberts, K. L., Lau, J. K., Chechlacz, M. & Humphreys, G. W. Spatial and temporal attention deficits following brain injury: a neuroanatomical decomposition of the temporal order judgement task. Cogn. Neuropsychol. 29, 300–324 (2012).
Mesulam, M. M. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Phil. Trans. R. Soc. Lond. B 354, 1325–1346 (1999).
Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).
Jaskowski, P. in Subjective Time: The Philosophy, Psychology and Neuroscience of Temporality (eds. Arstila, V. & Lloyd, D.) 379–407 (MIT Press, 2015).
Coull, J. T. & Nobre, A. C. 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, 7426–7435 (1998).
Wiener, M., Turkeltaub, P. E. & Coslett, H. B. Implicit timing activates the left inferior parietal cortex. Neuropsychologia 48, 3967–3971 (2010).
Nobre, A. C. & van Ede, F. Anticipated moments: temporal structure in attention. Nat. Rev. Neurosci. 19, 34–48 (2018).
Assmus, A. et al. Left inferior parietal cortex integrates time and space during collision judgments. Neuroimage 20, S82–S88 (2003).
Field, D. T. & Wann, J. P. Perceiving time to collision activates the sensorimotor cortex. Curr. Biol. 15, 453–458 (2005).
Coull, J. T., Vidal, F., Goulon, C., Nazarian, B. & Craig, C. Using time-to-contact information to assess potential collision modulates both visual and temporal prediction networks. Front. Hum. Neurosci. 2, 10 (2008).
Bolger, D., Coull, J. T. & Schön, D. Metrical rhythm implicitly orients attention in time as indexed by improved target detection and left inferior parietal activation. J. Cogn. Neurosci. 26, 593–605 (2014).
Morillon, B. & Baillet, S. Motor origin of temporal predictions in auditory attention. Proc. Natl Acad. Sci. USA 114, E8913–E8921 (2017).
Orpella, J. et al. Integrating when and what information in the left parietal lobe allows language rule generalization. PLoS Biol. 18, e3000895 (2020).
Cotti, J., Rohenkohl, G., Stokes, M., Nobre, A. C. & Coull, J. T. Functionally dissociating temporal and motor components of response preparation in left intraparietal sulcus. Neuroimage 54, 1221–1230 (2011).
Albouy, P., Benjamin, L., Morillon, B. & Zatorre, R. J. Distinct sensitivity to spectrotemporal modulation supports brain asymmetry for speech and melody. Science 367, 1043–1047 (2020).
Floegel, M., Fuchs, S. & Kell, C. A. Differential contributions of the two cerebral hemispheres to temporal and spectral speech feedback control. Nat. Commun. 11, 2839 (2020).
Droit-Volet, S., Trahanias, P. & Maniadakis, M. Passage of time judgments in everyday life are not related to duration judgments except for long durations of several minutes. Acta Psychol. 173, 116–121 (2017).
Droit-Volet, S. & Wearden, J. Passage of time judgments are not duration judgments: evidence from a study using experience sampling methodology. Front. Psychol. 7, 176 (2016).
Piras, F. & Coull, J. T. Implicit, predictive timing draws upon the same scalar representation of time as explicit timing. PLoS ONE 6, e18203 (2011).
Droit-Volet, S. & Coull, J. T. Distinct developmental trajectories for explicit and implicit timing. J. Exp. Child Psychol. 150, 141–154 (2016).
Ivry, R. B. & Hazeltine, R. E. Perception and production of temporal intervals across a range of durations: evidence for a common timing mechanism. J. Exp. Psychol. Hum. Percept. Perform. 21, 3–18 (1995).
Merchant, H., Zarco, W. & Prado, L. Do we have a common mechanism for measuring time in the hundreds of millisecond range? Evidence from multiple-interval timing tasks. J. Neurophysiol. 99, 939–949 (2008).
Buonomano, D. V., Bramen, J. & Khodadadifar, M. Influence of the interstimulus interval on temporal processing and learning: testing the state-dependent network model. Phil. Trans. R. Soc. B 364, 1865–1873 (2009).
Spencer, R. M., Karmarkar, U. & Ivry, R. B. Evaluating dedicated and intrinsic models of temporal encoding by varying context. Phil. Trans. R. Soc. B 364, 1853–1863 (2009).
Rammsayer, T. H., Borter, N. & Troche, S. J. Visual-auditory differences in duration discrimination of intervals in the subsecond and second range. Front. Psychol. 6, 1626 (2015).
Rammsayer, T. & Pichelmann, S. Visual-auditory differences in duration discrimination depend on modality-specific, sensory-automatic temporal processing: converging evidence for the validity of the sensory-automatic timing hypothesis. Q. J. Exp. Psychol. 71, 2364–2377 (2018).
Michon, J. A. in Time, Mind, and Behavior (eds Michon, J. A. & Jackson, J. L.) 20–54 (Springer, 1985).
Broadway, J. M. & Engle, R. W. Individual differences in working memory capacity and temporal discrimination. PLoS ONE 6, e25422 (2011).
Ogden, R. S., Samuels, M., Simmons, F., Wearden, J. & Montgomery, C. The differential recruitment of short-term memory and executive functions during time, number, and length perception: an individual differences approach. Q. J. Exp. Psychol. 71, 657–669 (2018).
Droit-Volet, S. Development of time. Curr. Opin. Behav. Sci. 8, 102–109 (2016).
Droit-Volet, S., Wearden, J. H. & Zélanti, P. S. Cognitive abilities required in time judgment depending on the temporal tasks used: a comparison of children and adults. Q. J. Exp. Psychol. 68, 2216–2242 (2015).
Matthews, W. J. & Meck, W. H. Temporal cognition: connecting subjective time to perception, attention, and memory. Psychol. Bull. 142, 865–907 (2016).
Macar, F., Grondin, S. & Casini, L. Controlled attention sharing influences time estimation. Mem. Cogn. 22, 673–686 (1994).
Xuan, B., Zhang, D., He, S. & Chen, X. Larger stimuli are judged to last longer. J. Vis. 7, 1–5 (2007).
Brown, S. W. Time, change, and motion: the effects of stimulus movement on temporal perception. Percept. Psychophys. 57, 105–116 (1995).
Tse, P. U., Intriligator, J., Rivest, J. & Cavanagh, P. Attention and the subjective expansion of time. Percept. Psychophys. 66, 1171–1189 (2004).
Matthews, W. J., Stewart, N. & Wearden, J. H. Stimulus intensity and the perception of duration. J. Exp. Psychol. Hum. Percept. Perform. 37, 303–313 (2011).
Droit-Volet, S. & Meck, W. H. How emotions colour our perception of time. Trends Cogn. Sci. 11, 504–513 (2007).
Jazayeri, M. & Shadlen, M. N. Temporal context calibrates interval timing. Nat. Neurosci. 13, 1020–1026 (2010).
Rhodes, D. On the distinction between perceived duration and event timing: towards a unified model of time perception. Timing Time Percept. 6, 90–123 (2018).
Ivry, R. B. & Keele, S. W. Timing functions of the cerebellum. J. Cogn. Neurosci. 1, 136–152 (1989).
Bareš, M. et al. Consensus paper: decoding the contributions of the cerebellum as a time machine. From neurons to clinical applications. Cerebellum 18, 266–286 (2019).
Breska, A. & Ivry, R. B. Double dissociation of single-interval and rhythmic temporal prediction in cerebellar degeneration and Parkinson’s disease. Proc. Natl Acad. Sci. USA 115, 12283–12288 (2018).
Jones, C. R. & Jahanshahi, M. Contributions of the basal ganglia to temporal processing: evidence from Parkinson’s disease. Timing Time Percept. 2, 87–127 (2014).
Gouvêa, T. S. et al. Striatal dynamics explain duration judgments. eLife 4, e11386 (2015).
Gu, B. M., Kukreja, K. & Meck, W. H. Oscillation patterns of local field potentials in the dorsal striatum and sensorimotor cortex during the encoding, maintenance, and decision stages for the ordinal comparison of sub- and supra-second signal durations. Neurobiol. Learn. Mem. 153, 79–91 (2018).
Casini, L. & Ivry, R. B. Effects of divided attention on temporal processing in patients with lesions of the cerebellum or frontal lobe. Neuropsychology 13, 10–21 (1999).
Mangels, J. A., Ivry, R. B. & Shimizu, N. Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Brain Res. Cogn. Brain Res. 7, 15–39 (1998).
Coull, J. T., Charras, P., Donadieu, M., Droit-Volet, S. & Vidal, F. SMA selectively codes the active accumulation of temporal, not spatial, magnitude. J. Cogn. Neurosci. 27, 2281–2298 (2015).
Schwartze, M., Rothermich, K. & Kotz, S. A. Functional dissociation of pre-SMA and SMA-proper in temporal processing. Neuroimage 60, 290–298 (2012).
Nani, A. et al. The neural correlates of time: a meta-analysis of neuroimaging studies. J. Cogn. Neurosci. 31, 1796–1826 (2019).
Tipples, J., Brattan, V. & Johnston, P. Neural bases for individual differences in the subjective experience of short durations (less than 2 seconds). PLoS ONE 8, e54669 (2013).
Mita, A., Mushiake, H., Shima, K., Matsuzaka, Y. & Tanji, J. Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat. Neurosci. 12, 502–507 (2009).
Merchant, H., Zarco, W., Pérez, O., Prado, L. & Bartolo, R. Measuring time with different neural chronometers during a synchronization-continuation task. Proc. Natl Acad. Sci. USA 108, 19784–19789 (2011).
Crowe, D. A., Zarco, W., Bartolo, R. & Merchant, H. Dynamic representation of the temporal and sequential structure of rhythmic movements in the primate medial premotor cortex. J. Neurosci. 34, 11972–11983 (2014).
Henry, M. J., Herrmann, B. & Obleser, J. Selective attention to temporal features on nested time scales. Cereb. Cortex 25, 450–459 (2015).
Mento, G., Tarantino, V., Sarlo, M. & Bisiacchi, P. S. Automatic temporal expectancy: a high-density event-related potential study. PLoS ONE 8, e62896 (2013).
Coull, J. T., Vidal, F., Nazarian, B. & Macar, F. Functional anatomy of the attentional modulation of time estimation. Science 303, 1506–1508 (2004).
Merchant, H., Pérez, O., Zarco, W. & Gámez, J. Interval tuning in the primate medial premotor cortex as a general timing mechanism. J. Neurosci. 33, 9082–9096 (2013).
Mendoza, G., Méndez, J. C., Pérez, O., Prado, L. & Merchant, H. Neural basis for categorical boundaries in the primate pre-SMA during relative categorization of time intervals. Nat. Commun. 9, 1098 (2018).
Protopapa, F. et al. Chronotopic maps in human supplementary motor area. PLoS Biol. 17, e3000026 (2019).
Hayashi, M. J. et al. Time adaptation shows duration selectivity in the human parietal cortex. PLoS Biol. 13, e1002262 (2015).
Hayashi, M. J. & Ivry, R. B. Duration selectivity in right parietal cortex reflects the subjective experience of time. J. Neurosci. 40, 7749–7758 (2020).
Harvey, B. M., Dumoulin, S. O., Fracasso, A. & Paul, J. M. A network of topographic maps in human association cortex hierarchically transforms visual timing-selective responses. Curr. Biol. 30, 1424–1434.e6 (2020).
Bueti, D. Time processing: multiple topographic representations of time across human cortex. Curr. Biol. 30, R356–R358 (2020).
Kononowicz, T. W. & van Rijn, H. Decoupling interval timing and climbing neural activity: a dissociation between CNV and N1P2 amplitudes. J. Neurosci. 34, 2931–2939 (2014).
Coull, J. T. & Droit-Volet, S. Explicit understanding of duration develops implicitly through action. Trends Cogn. Sci. 22, 923–937 (2018).
Coull, J. T., Hwang, H. J., Leyton, M. & Dagher, A. Dopamine precursor depletion impairs timing in healthy volunteers by attenuating activity in putamen and supplementary motor area. J. Neurosci. 32, 16704–16715 (2012).
Maricq, A. V. & Church, R. M. The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology 79, 10–15 (1983).
Meck, W. H. Neuropharmacology of timing and time perception. Brain Res. Cogn. Brain Res. 3, 227–242 (1996).
Soares, S., Atallah, B. V. & Paton, J. J. Midbrain dopamine neurons control judgment of time. Science 354, 1273–1277 (2016).
Rammsayer, T. H. Are there dissociable roles of the mesostriatal and mesolimbocortical dopamine systems on temporal information processing in humans? Neuropsychobiology 35, 36–45 (1997).
Rammsayer, T. H. Neuropharmacological evidence for different timing mechanisms in humans. Q. J. Exp. Psychol. B 52, 273–286 (1999).
Rakitin, B. C., Scarmeas, N., Li, T., Malapani, C. & Stern, Y. Single-dose levodopa administration and aging independently disrupt time production. J. Cogn. Neurosci. 18, 376–387 (2006).
Lake, J. I. & Meck, W. H. Differential effects of amphetamine and haloperidol on temporal reproduction: dopaminergic regulation of attention and clock speed. Neuropsychologia 51, 284–292 (2013).
Coull, J. T., Hwang, H. J., Leyton, M. & Dagher, A. Dopaminergic modulation of motor timing in healthy volunteers differs as a function of baseline DA precursor availability. Timing Time Percept. 1, 77–98 (2013).
Tomassini, A., Ruge, D., Galea, J. M., Penny, W. & Bestmann, S. The role of dopamine in temporal uncertainty. J. Cogn. Neurosci. 28, 96–110 (2016).
Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381 (1986).
Rammsayer, T. H. Effects of pharmacologically induced dopamine-receptor stimulation on human temporal information processing. Neuroquantology 7, 103–113 (2009).
White, T. P. et al. Eluding the illusion? Schizophrenia, dopamine and the McGurk effect. Front. Hum. Neurosci. 8, 565 (2014).
Chassignolle, M. et al. Dopamine precursor depletion in healthy volunteers impairs processing of duration but not temporal order. J. Cogn. Neurosci. 33, 946–963 (2021).
Cools, R., Froböse, M., Aarts, E. & Hofmans, L. Dopamine and the motivation of cognitive control. Handb. Clin. Neurol. 163, 123–143 (2019).
Allman, M. J. & Meck, W. H. Pathophysiological distortions in time perception and timed performance. Brain 135, 656–677 (2012).
Blom, J. D., Nanuashvili, N. & Waters, F. Time distortions: a systematic review of cases characteristic of Alice in Wonderland syndrome. Front. Psychiat. 12, 668633 (2021).
Farmer, M. E. & Klein, R. M. The evidence for a temporal processing deficit linked to dyslexia: a review. Psychon. Bull. Rev. 2, 460–493 (1995).
Foss-Feig, J. H. et al. An extended multisensory temporal binding window in autism spectrum disorders. Exp. Brain Res. 203, 381–389 (2010).
Stevenson, R. A. et al. Multisensory temporal integration in autism spectrum disorders. J. Neurosci. 34, 691–697 (2014).
Wallace, M. T. & Stevenson, R. A. The construct of the multisensory temporal binding window and its dysregulation in developmental disabilities. Neuropsychologia 64, 105–123 (2014).
Meilleur, A., Foster, N., Coll, S. M., Brambati, S. M. & Hyde, K. L. Unisensory and multisensory temporal processing in autism and dyslexia: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 116, 44–63 (2020).
Laasonen, M., Service, E. & Virsu, V. Temporal order and processing acuity of visual, auditory, and tactile perception in developmentally dyslexic young adults. Cogn. Affect. Behav. Neurosci. 1, 394–410 (2001).
Kwakye, L. D., Foss-Feig, J. H., Cascio, C. J., Stone, W. L. & Wallace, M. T. Altered auditory and multisensory temporal processing in autism spectrum disorders. Front. Integr. Neurosci. 4, 129 (2011).
Noreika, V., Falter, C. M. & Rubia, K. Timing deficits in attention-deficit/hyperactivity disorder (ADHD): evidence from neurocognitive and neuroimaging studies. Neuropsychologia 51, 235–266 (2013).
American Psychiatric Association. DSM-5: Diagnostic and Statistical Manual of Mental Disorders 5th edn (APA, 2013).
McCutcheon, R. A., Reis Marques, T. & Howes, O. D. Schizophrenia — an overview. JAMA Psychiat. 77, 201–210 (2020).
Fuchs, T. & Van Duppen, Z. Time and events: on the phenomenology of temporal experience in schizophrenia. Psychopathology 50, 68–74 (2017).
Minkowski, E. Le Temps Vécu: Etudes Phénoménologiques et Psychopathologiques (Presses Universitaires de France, 1933).
Stanghellini, G. et al. Psychopathology of lived time: abnormal time experience in persons with schizophrenia. Schizophren. Bull. 42, 45–55 (2016).
Zhou, H. Y. et al. Multisensory temporal binding window in autism spectrum disorders and schizophrenia spectrum disorders: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 86, 66–76 (2018).
Giersch, A. et al. Extended visual simultaneity thresholds in patients with schizophrenia. Schizophr. Bull. 35, 816–825 (2009).
Schmidt, H., McFarland, J., Ahmed, M., McDonald, C. & Elliott, M. A. Low-level temporal coding impairments in psychosis: preliminary findings and recommendations for further studies. J. Abnorm. Psychol. 120, 476–482 (2011).
Foucher, J. R., Lacambre, M., Pham, B. T., Giersch, A. & Elliott, M. A. Low time resolution in schizophrenia: lengthened windows of simultaneity for visual, auditory and bimodal stimuli. Schizophr. Res. 97, 118–127 (2007).
Di Cosmo, G. et al. Body-environment integration: temporal processing of tactile and auditory inputs along the schizophrenia continuum. J. Psychiat. Res. 134, 208–214 (2021).
Stevenson, R. A. et al. The associations between multisensory temporal processing and symptoms of schizophrenia. Schizophr. Res. 179, 97–103 (2017).
Noel, J. P., Stevenson, R. A. & Wallace, M. T. Atypical audiovisual temporal function in autism and schizophrenia: similar phenotype, different cause. Eur. J. Neurosci. 47, 1230–1241 (2018).
Voss, M. et al. Altered awareness of action in schizophrenia: a specific deficit in predicting action consequences. Brain 133, 3104–3112 (2010).
Capa, R. L., Duval, C. Z., Blaison, D. & Giersch, A. Patients with schizophrenia selectively impaired in temporal order judgments. Schizophr. Res. 156, 51–55 (2014).
de Boer-Schellekens, L., Stekelenburg, J. J., Maes, J. P., Van Gool, A. R. & Vroomen, J. Sound improves diminished visual temporal sensitivity in schizophrenia. Acta Psychol. 147, 136–142 (2014).
Su, L. et al. Temporal perception deficits in schizophrenia: integration is the problem, not deployment of attentions. Sci. Rep. 5, 9745 (2015).
Del Cul, A., Dehaene, S. & Leboyer, M. Preserved subliminal processing and impaired conscious access in schizophrenia. Arch. Gen. Psychiat. 63, 1313–1323 (2006).
Berkovitch, L., Dehaene, S. & Gaillard, R. Disruption of conscious access in schizophrenia. Trends Cogn. Sci. 21, 878–892 (2017).
Giersch, A. et al. Disruption of information processing in schizophrenia: the time perspective. Schizophr. Res. Cogn. 2, 78–83 (2015).
Giersch, A. in The Illusions of Time (eds Arstila, V., Bardon, A., Power, S. & Vatakis, A.) 205–223 (Palgrave Macmillan, 2019).
Marques-Carneiro, J. E., Krieg, J., Duval, C. Z., Schwitzer, T. & Giersch, A. Paradoxical sensitivity to sub-threshold asynchronies in schizophrenia: a behavioural and EEG approach. Schizophren. Bull. Open 2, sgab011 (2021).
Foerster, F. R. et al. Volatility of subliminal haptic feedback alters the feeling of control in schizophrenia. J. Abnorm. Psychol. 130, 775–784 (2021).
Freedman, B. J. The subjective experience of perceptual and cognitive disturbances in schizophrenia: a review of autobiographical accounts. Arch. Gen. Psychiat. 30, 333–340 (1974).
Ciullo, V., Spalletta, G., Caltagirone, C., Jorge, R. E. & Piras, F. Explicit time deficit in schizophrenia: systematic review and meta-analysis indicate it is primary and not domain specific. Schizophren. Bull. 42, 505–518 (2016).
Peterburs, J., Nitsch, A. M., Miltner, W. H. & Straube, T. Impaired representation of time in schizophrenia is linked to positive symptoms and cognitive demand. PLoS ONE 8, e67615 (2013).
Davalos, D. B., Kisley, M. A. & Freedman, R. Behavioral and electrophysiological indices of temporal processing dysfunction in schizophrenia. J. Neuropsychiat. Clin. Neurosci. 17, 517–525 (2005).
Davalos, D. B., Rojas, D. C. & Tregellas, J. R. Temporal processing in schizophrenia: effects of task-difficulty on behavioral discrimination and neuronal responses. Schizophren. Res. 127, 123–130 (2011).
Elvevåg, B. et al. Duration judgements in patients with schizophrenia. Psychol. Med. 33, 1249–1261 (2003).
Carroll, C. A., O’Donnell, B. F., Shekhar, A. & Hetrick, W. P. Timing dysfunctions in schizophrenia as measured by a repetitive finger tapping task. Brain Cogn. 71, 345–353 (2009).
Lee, K. H. et al. Time perception and its neuropsychological correlates in patients with schizophrenia and in healthy volunteers. Psychiat. Res. 166, 174–183 (2009).
Roy, M., Grondin, S. & Roy, M. A. Time perception disorders are related to working memory impairment in schizophrenia. Psychiat. Res. 200, 159–166 (2012).
de Montalembert, M., Coulon, N., Cohen, D., Bonnot, O. & Tordjman, S. Time perception of simultaneous and sequential events in early-onset schizophrenia. Neurocase 22, 392–399 (2016).
Ciullo, V. et al. Predictive timing disturbance is a precise marker of schizophrenia. Schizophren. Res. Cogn. 12, 42–49 (2018).
Michie, P. T. et al. Duration and frequency mismatch negativity in schizophrenia. Clin. Neurophysiol. 111, 1054–1065 (2000).
Umbricht, D. & Krljes, S. Mismatch negativity in schizophrenia: a meta-analysis. Schizophren. Res. 76, 1–23 (2005).
Erickson, M. A., Ruffle, A. & Gold, J. M. A meta-analysis of mismatch negativity in schizophrenia: from clinical risk to disease specificity and progression. Biol. Psychiat. 79, 980–987 (2016).
Suga, M., Nishimura, Y., Kawakubo, Y., Yumoto, M. & Kasai, K. Magnetoencephalographic recording of auditory mismatch negativity in response to duration and frequency deviants in a single session in patients with schizophrenia. Psychiat. Clin. Neurosci. 70, 295–302 (2016).
Näätänen, R. et al. The mismatch negativity (MMN) — a unique window to disturbed central auditory processing in ageing and different clinical conditions. Clin. Neurophysiol. 123, 424–458 (2012).
Lieder, F., Stephan, K. E., Daunizeau, J., Garrido, M. I. & Friston, K. J. A neurocomputational model of the mismatch negativity. PLoS Comput. Biol. 9, e1003288 (2013).
Wacongne, C. A predictive coding account of MMN reduction in schizophrenia. Biol. Psychol. 116, 68–74 (2016).
Adams, R. A., Stephan, K. E., Brown, H. R., Frith, C. D. & Friston, K. J. The computational anatomy of psychosis. Front. Psychiat. 4, 47 (2013).
Friston, K. J. The free energy principle: a unified brain theory? Nat. Rev. Neurosci. 11, 127–138 (2010).
Notredame, C. E., Pins, D., Deneve, S. & Jardri, R. What visual illusions teach us about schizophrenia. Front. Integr. Neurosci. 8, 63 (2014).
Sterzer, P. et al. The predictive coding account of psychosis. Biol. Psychiat. 84, 634–643 (2018).
Martin, B. et al. Fragile temporal prediction in patients with schizophrenia is related to minimal self disorders. Sci. Rep. 7, 8278 (2017).
Delevoye-Turrell, Y., Wilquin, H. & Giersch, A. A ticking clock for the production of sequential actions: where does the problem lie in schizophrenia? Schizophren. Res. 135, 51–54 (2012).
Wilquin, H., Delevoye-Turrell, Y., Dione, M. & Giersch, A. Motor synchronization in patients with schizophrenia: preserved time representation with abnormalities in predictive timing. Front. Hum. Neurosci. 12, 193 (2018).
Horacek, M., Kärgel, C., Scherbaum, N. & Müller, B. W. The effect of deviance predictability on mismatch negativity in schizophrenia patients. Neurosci. Lett. 617, 76–81 (2016).
Hay, R. A. et al. Equivalent mismatch negativity deficits across deviant types in early illness schizophrenia-spectrum patients. Biol. Psychol. 105, 130–137 (2015).
Beck, K. et al. Association of ketamine with psychiatric symptoms and implications for its therapeutic use and for understanding schizophrenia: a systematic review and meta-analysis. JAMA Netw. Open 3, e204693 (2020).
Vinogradov, S. Has the time come for cognitive remediation in schizophrenia…again? Am. J. Psychiatry 176, 262–264 (2019).
Parker, K. et al. Delta-frequency stimulation of cerebellar projections can compensate for schizophrenia-related medial frontal dysfunction. Mol. Psychiat. 22, 647–655 (2017).
Stocco, A. Coordinate-based meta-analysis of fMRI studies with R. R J. 6, 5–15 (2014).
Poncelet, P. E. & Giersch, A. Tracking visual events in time in the absence of time perception: implicit processing at the ms level. PLoS ONE 10, e0127106 (2015).
Chassignolle, M., Giersch, A. & Coull, J. T. Evidence for visual temporal order processing below the threshold for conscious perception. Cognition 207, 104528 (2021).
Long, J. M. & Kesner, R. P. Phencyclidine impairs temporal order memory for spatial locations in rats. Pharmacol. Biochem. Behav. 52, 645–648 (1995).
Marquis, J. P., Goulet, S. & Doré, F. Y. Schizophrenia-like syndrome inducing agent phencyclidine failed to impair memory for temporal order in rats. Neurobiol. Learn. Mem. 80, 158–167 (2003).
Lins, B. R., Ballendine, S. A. & Howland, J. G. Altered object exploration but not temporal order memory retrieval in an object recognition test following treatment of rats with the group II metabotropic glutamate receptor agonist LY379268. Neurosci. Lett. 560, 41–45 (2014).
Coull, J. T. et al. Ketamine perturbs perception of the flow of time in healthy volunteers. Psychopharmacology 218, 543–556 (2011).
Rosburg, T. & Kreitschmann-Andermahr, I. The effects of ketamine on the mismatch negativity (MMN) in humans — a meta-analysis. Clin. Neurophysiol. 127, 1387–1394 (2016).
Harms, L., Parras, G. G., Michie, P. T. & Malmierca, M. S. The role of glutamate neurotransmission in mismatch negativity (MMN), a measure of auditory synaptic plasticity and change-detection. Neuroscience 456, 106–113 (2021).
Greenwood, L. M. et al. The effects of glycine on auditory mismatch negativity in schizophrenia. Schizophren. Res. 191, 61–69 (2018).
Lavoie, S. et al. Glutathione precursor, N-acetyl-cysteine, improves mismatch negativity in schizophrenia patients. Neuropsychopharmacology 33, 2187–2199 (2008).
Acknowledgements
The authors are co-funded by the Agence Nationale de la Recherche grant ANR-16-CE37-0004-02. They are grateful to M. Chassignolle for help preparing the images in Fig. 3.
Author information
Authors and Affiliations
Contributions
The authors contributed equally to all aspects of the article.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Reviews Psychology thanks Deana Davalos, Masamichi Hayashi and the other, anonymous, reviewer for their contribution to the peer review of this work.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Coull, J.T., Giersch, A. The distinction between temporal order and duration processing, and implications for schizophrenia. Nat Rev Psychol 1, 257–271 (2022). https://doi.org/10.1038/s44159-022-00038-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s44159-022-00038-y
This article is cited by
-
Neurocognitive analyses reveal that video game players exhibit enhanced implicit temporal processing
Communications Biology (2022)
