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Anticipated moments: temporal structure in attention

Key Points

  • Attention enables the prioritization and selection of relevant sensory inputs and appropriate responses. Understanding the cognitive and neural mechanisms by which attention is allocated to relevant moments in time provides a necessary complement to the study of spatial, feature-based and object-based attention.

  • At least four types of informative temporal structures enable temporal expectations to guide attention in time: cued associations, hazard rates, rhythms and sequences. Their impacts on perception and action need not always run through common mechanisms and may often interact.

  • Investigations of how temporal expectations are controlled and utilized by the brain are only beginning to gain ground but already suggest that there are multiple mechanisms at play, involving, among others, changes in the strength, timing and synchrony of neuronal activity.

  • Temporal expectations often co-occur with spatial and feature-based expectations, amplifying their impact on neural responses and performance. Accordingly, temporal expectations may often run through other, receptive-field-based, attentional biases.

  • Although the study of temporal attention takes its roots in the domains of perception and action, it is likely to be important across many cognitive domains (working memory, reinforcement learning and so on) and may contribute to a better understanding of many cognitive disorders.

Abstract

We have come to recognize the brain as a predictive organ, anticipating attributes of the incoming sensory stimulation to guide perception and action in the service of adaptive behaviour. In the quest to understand the neural bases of the modulatory prospective signals that prioritize and select relevant events during perception, one fundamental dimension has until recently been largely overlooked: time. In this Review, we introduce the burgeoning field of temporal attention and illustrate how the brain makes use of various forms of temporal regularities in the environment to guide adaptive behaviour and influence neural processing.

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Figure 1: Types of temporal structures.
Figure 2: Memory-guided temporal expectations.
Figure 3: Selective entrainment to relevant stimulus modality or feature.
Figure 4: Temporal expectations in working memory.

References

  1. Reynolds, J. H. & Chelazzi, L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27, 611–647 (2004).

    CAS  PubMed  Google Scholar 

  2. Cohen, M. R. & Maunsell, J. H. R. in The Oxford Handbook of Attention (eds Nobre, A. C. & Kastner, S.) 318–345 (Oxford Univ. Press, 2014).

    Google Scholar 

  3. Fries, P. Rhythms for cognition: communication through coherence. Neuron 88, 220–235 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Posner, M. I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

    CAS  Google Scholar 

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

    Google Scholar 

  6. Los, S. A. in Attention and Time (eds Nobre, A. C. & Coull, J. T.) 289–302 (Oxford Univ. Press, 2010).

    Google Scholar 

  7. 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). This is a landmark brain-imaging study in humans that reveals the brain network involved in temporal orienting of attention and compares and contrasts it with the spatial orienting network.

    CAS  PubMed  Google Scholar 

  8. Miniussi, C., Wilding, E. L., Coull, J. T. & Nobre, A. C. Orienting attention in time: modulation of brain potentials. Brain 122, 1507–1518 (1999).

    PubMed  Google Scholar 

  9. Griffin, I. C., Miniussi, C. & Nobre, A. C. Multiple mechanisms of selective attention: differential modulation of stimulus processing by attention to space or time. Neuropsychologia 40, 2325–2340 (2002).

    PubMed  Google Scholar 

  10. Auksztulewicz, R. & Friston, K. Attentional enhancement of auditory mismatch responses: a DCM/MEG study. Cereb. Cortex 25, 4273–4283 (2015).

    PubMed  PubMed Central  Google Scholar 

  11. Griffin, I. C., Miniussi, C. & Nobre, A. C. Orienting attention in time. Front. Biosci. 6, 660–671 (2001).

    Google Scholar 

  12. Correa, A. in Attention and Time (eds Nobre, A. C. & Coull, J. T.) 357–370 (Oxford Univ. Press, 2010).

    Google Scholar 

  13. Coull, J. T., Frith, C. D., Büchel, C. & Nobre, A. C. Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia 38, 808–819 (2000).

    CAS  PubMed  Google Scholar 

  14. Nobre, A. C. Orienting attention to instants in time. Neuropsychologia 39, 1317–1328 (2001).

    CAS  PubMed  Google Scholar 

  15. Lange, K. & Röder, B. Orienting attention to points in time improves stimulus processing both within and across modalities. J. Cogn. Neurosci. 18, 715–729 (2006).

    PubMed  Google Scholar 

  16. Anderson, B. & Sheinberg, D. L. Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex. Neuropsychologia 46, 947–957 (2008).

    PubMed  Google Scholar 

  17. Jaramillo, S. & Zador, A. M. The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nat. Neurosci. 14, 246–251 (2011). This study demonstrates the behavioural and neural benefits of cued temporal attention in a rodent model, such as temporally selective increases in A1 firing rate for neurons coding for the incoming stimuli to enhance the representation of sounds when auditory targets are expected.

    CAS  PubMed  Google Scholar 

  18. Denison, R. N., Heeger, D. J. & Carrasco, M. Attention flexibly trades off across points in time. Psychon Bull. Rev. 24, 1142–1151 (2017).

    PubMed  PubMed Central  Google Scholar 

  19. Chun, M. M. & Jiang, Y. Contextual cueing: implicit learning and memory of visual context guides spatial attention. Cogn. Psychol. 36, 28–71 (1998).

    CAS  PubMed  Google Scholar 

  20. Summerfield, J. J., Lepsien, J., Gitelman, D. R., Mesulam, M. M. & Nobre, A. C. Orienting attention based on long-term memory experience. Neuron 49, 905–916 (2006).

    CAS  PubMed  Google Scholar 

  21. Olson, I. R. & Chun, M. M. Temporal contextual cuing of visual attention. J. Exp. Psychol. Learn. Mem. Cogn. 27, 1299–1313 (2001).

    CAS  PubMed  Google Scholar 

  22. Cravo, A. M., Rohenkohl, G., Santos, K. M. & Nobre, A. C. Temporal anticipation based on memory. J. Cogn. Neurosci. 29, 2081–2089 (2017). This recent study in humans demonstrates that long-term memories carry temporal associations that guide perception through temporally selective anticipation of target stimuli.

    PubMed  PubMed Central  Google Scholar 

  23. Mattiesing, R. M., Kruijne, W., Meeter, M. & Los, S. A. Timing a week later: the role of long-term memory in temporal preparation. Psychonom. Bull. Rev. http://dx.doi.org/10.3758/s13423-017-1270-3 (2017).

  24. Luce, R. D. Response Times: Their Role in Inferring Elementary Mental Organization. (Oxford Univ. Press; Clarendon Press, 1986).

    Google Scholar 

  25. Schoffelen, J.-M., Oostenveld, R. & Fries, P. Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308, 111–113 (2005).

    CAS  PubMed  Google Scholar 

  26. Cravo, A. M., Rohenkohl, G., Wyart, V. & Nobre, A. C. Endogenous modulation of low frequency oscillations by temporal expectations. J. Neurophysiol. 106, 2964–2972 (2011).

    PubMed  PubMed Central  Google Scholar 

  27. Vangkilde, S., Petersen, A. & Bundesen, C. Temporal expectancy in the context of a theory of visual attention. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20130054 (2013).

    PubMed  PubMed Central  Google Scholar 

  28. Ghose, G. M. & Maunsell, J. H. R. Attentional modulation in visual cortex depends on task timing. Nature 419, 616–620 (2002). This study presents a seminal demonstration in NHPs that attentional modulation of neuronal firing rates in a visual area (V4) follows the temporal hazard rate for the occurrence of target stimuli.

    CAS  PubMed  Google Scholar 

  29. Janssen, P. & Shadlen, M. N. A representation of the hazard rate of elapsed time in macaque area LIP. Nat. Neurosci. 8, 234–242 (2005).

    CAS  PubMed  Google Scholar 

  30. de Hemptinne, C., Nozaradan, S., Duvivier, Q., Lefevre, P. & Missal, M. How do primates anticipate uncertain future events? J. Neurosci. 27, 4334–4341 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Barnes, R. & Jones, M. R. Expectancy, attention, and time. Cogn. Psychol. 41, 254–311 (2000).

    CAS  PubMed  Google Scholar 

  32. Jones, M. R., Johnston, H. M. & Puente, J. Effects of auditory pattern structure on anticipatory and reactive attending. Cogn. Psychol. 53, 59–96 (2006).

    PubMed  Google Scholar 

  33. Jones, M. R. Time, our lost dimension: toward a new theory of perception, attention, and memory. Psychol. Rev. 83, 323–355 (1976). This is an early theoretical and review paper from the auditory-perception literature stressing the important role of temporal structures in attention.

    CAS  PubMed  Google Scholar 

  34. Large, E. W. & Jones, M. R. The dynamics of attending. Psychol. Rev. 106, 119–159 (1999).

    Google Scholar 

  35. Lawrance, E. L. A., Harper, N. S., Cooke, J. E. & Schnupp, J. W. H. Temporal predictability enhances auditory detection. J. Acoust. Soc. Am. 135, EL357–EL363 (2014).

    PubMed  PubMed Central  Google Scholar 

  36. Sanabria, D., Capizzi, M. & Correa, A. Rhythms that speed you up. J. Exp. Psychol. Hum. Percept. Perform. 37, 236–244 (2011).

    PubMed  Google Scholar 

  37. Mathewson, K. E., Fabiani, M., Gratton, G., Beck, D. M. & Lleras, A. Rescuing stimuli from invisibility: inducing a momentary release from visual masking with pre-target entrainment. Cognition 115, 186–191 (2010).

    PubMed  Google Scholar 

  38. Cravo, A. M., Rohenkohl, G., Wyart, V. & Nobre, A. C. Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex. J. Neurosci. 33, 4002–4010 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Rohenkohl, G., Cravo, A. M., Wyart, V. & Nobre, A. C. Temporal expectation improves the quality of sensory information. J. Neurosci. 32, 8424–8428 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Palmer, J., Huk, A. C. & Shadlen, M. N. The effect of stimulus strength on the speed and accuracy of a perceptual decision. J. Vision 5, 376–404 (2005).

    Google Scholar 

  41. Breska, A. & Deouell, L. Y. Automatic bias of temporal expectations following temporally regular input independently of high-level temporal expectation. J. Cogn. Neurosci. 26, 1555–1571 (2014). This is a study in humans that offers a clear demonstration that different types of temporal structures can have dissociable impacts on perception.

    PubMed  Google Scholar 

  42. Nissen, M. J. & Bullemer, P. Attention requirements of learning: evidence from performance measures. Cogn. Psychol. 19, 1–32 (1987).

    Google Scholar 

  43. Reed, J. & Johnson, P. Assessing implicit learning with indirect tests. J. Exp. Psychol. Learn. Mem. Cogn. 20, 585–594 (1994).

    Google Scholar 

  44. Shin, J. C. & Ivry, R. B. Concurrent learning of temporal and spatial sequences. Learn. Mem. 28, 445–457 (2002).

    Google Scholar 

  45. O'Reilly, J. X., McCarthy, K. J., Capizzi, M. & Nobre, A. C. Acquisition of the temporal and ordinal structure of movement sequences in incidental learning. J. Neurophysiol. 99, 2731–2735 (2008).

    PubMed  Google Scholar 

  46. Heideman, S. G., van Ede, F. & Nobre, A. C. Temporal alignment of anticipatory motor cortical beta lateralisation in hidden visual-motor sequences. Eur. J. Neurosci. http://dx.doi.org/10.1111/ejn.13700 (2017). This study in humans shows that complex, non-isochronous, temporal sequences are utilized by the brain to align motor preparation to anticipated moments in time.

  47. Heideman, S. G., van Ede, F. & Nobre, A. C. Early behavioural facilitation by temporal expectations in complex visual-motor sequences. J. Physiol. Paris http://dx.doi.org/10.1016/j.jphysparis.2017.03.003 (2017).

  48. Rohenkohl, G., Coull, J. T. & Nobre, A. C. Behavioural dissociation between exogenous and endogenous temporal orienting of attention. PLoS ONE 6, e14620 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Capizzi, M., Correa, A. & Sanabria, D. Temporal orienting of attention is interfered by concurrent working memory updating. Neuropsychologia 51, 326–339 (2013).

    PubMed  Google Scholar 

  50. Capizzi, M., Sanabria, D. & Correa, Á. Dissociating controlled from automatic processing in temporal preparation. Cognition 123, 293–302 (2012).

    PubMed  Google Scholar 

  51. de la Rosa, M. D., Sanabria, D., Capizzi, M. & Correa, A. Temporal preparation driven by rhythms is resistant to working memory interference. Front. Psychol. 3, 308–317 (2012).

    PubMed  PubMed Central  Google Scholar 

  52. Correa, Á., Cona, G., Arbula, S., Vallesi, A. & Bisiacchi, P. Neural dissociation of automatic and controlled temporal preparation by transcranial magnetic stimulation. Neuropsychologia 65, 131–136 (2014).

    PubMed  Google Scholar 

  53. Triviño, M., Correa, Á., Arnedo, M. & Lupiáñez, J. Temporal orienting deficit after prefrontal damage. Brain 133, 1173–1185 (2010).

    PubMed  Google Scholar 

  54. Triviño, M., Arnedo, M., Lupiáñez, J., Chirivella, J. & Correa, Á. Rhythms can overcome temporal orienting deficit after right frontal damage. Neuropsychologia 49, 3917–3930 (2011).

    PubMed  Google Scholar 

  55. Correa, A. & Nobre, A. C. Neural modulation by regularity and passage of time. J. Neurophysiol. 100, 1649–1655 (2008).

    PubMed  Google Scholar 

  56. Ossmy, O. et al. The timescale of perceptual evidence integration can be adapted to the environment. Curr. Biol. 23, 981–986 (2013).

    CAS  PubMed  Google Scholar 

  57. Murphy, P. R., Boonstra, E. & Nieuwenhuis, S. Global gain modulation generates time-dependent urgency during perceptual choice in humans. Nat. Commun. 7, 13526 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Lerner, Y., Honey, C. J., Katkov, M. & Hasson, U. Temporal scaling of neural responses to compressed and dilated natural speech. J. Neurophysiol. 111, 2433–2444 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Ding, N., Melloni, L., Zhang, H., Tian, X. & Poeppel, D. Cortical tracking of hierarchical linguistic structures in connected speech. Nat. Neurosci. 19, 158–164 (2016).

    CAS  PubMed  Google Scholar 

  60. Muller, T. & Nobre, A. C. Perceiving the passage of time: neural possibilities. Ann. NY Acad. Sci. 1326, 60–71 (2014).

    PubMed  Google Scholar 

  61. Merchant, H., Harrington, D. L. & Meck, W. H. Neural basis of the perception and estimation of time. Annu. Rev. Neurosci. 36, 313–336 (2013).

    CAS  PubMed  Google Scholar 

  62. Goel, A. & Buonomano, D. V. Timing as an intrinsic property of neural networks: evidence from in vivo and in vitro experiments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120460 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. Theunissen, F. E., Sen, K. & Doupe, A. J. Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J. Neurosci. 20, 2315–2331 (2000).

    CAS  PubMed  Google Scholar 

  64. Eichenbaum, H. Time cells in the hippocampus: a new dimension for mapping memories. Nat. Rev. Neurosci. 15, 732–744 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Wiener, M., Turkeltaub, P. & Coslett, H. B. The image of time: a voxel-wise meta-analysis. Neuroimage 49, 1728–1740 (2010).

    PubMed  Google Scholar 

  66. Nobre, A. C. & Rohenkohl, G. in The Oxford Handbook of Attention (eds Nobre, A. C. & Kastner, S.) 676–724 (Oxford Univ. Press, 2014).

    Google Scholar 

  67. 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).

    PubMed  Google Scholar 

  68. Coull, J. T., Cotti, J. & Vidal, F. Differential roles for parietal and frontal cortices in fixed versus evolving temporal expectations: dissociating prior from posterior temporal probabilities with fMRI. Neuroimage 141, 40–51 (2016).

    PubMed  Google Scholar 

  69. Schubotz, R. I. Prediction of external events with our motor system: towards a new framework. Trends Cogn. Sci. 11, 211–218 (2007).

    PubMed  Google Scholar 

  70. Morillon, B., Schroeder, C. E. & Wyart, V. Motor contributions to the temporal precision of auditory attention. Nat. Commun. 5, 5255 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F. & Weisz, D. J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100, 729–744 (1986).

    CAS  PubMed  Google Scholar 

  72. Clark, R. E. & Squire, L. R. Classical conditioning and brain systems: the role of awareness. Science 280, 77–81 (1998).

    CAS  PubMed  Google Scholar 

  73. Friston, K. & Buzsáki, G. The functional anatomy of time: what and when in the brain. Trends Cogn. Sci. 7, 500–511 (2016).

    Google Scholar 

  74. Ólafsdóttir, H. F., Barry, C., Saleem, A. B., Hassabis, D. & Spiers, H. J. Hippocampal place cells construct reward related sequences through unexplored space. eLife 4, e06063 (2015).

    PubMed  PubMed Central  Google Scholar 

  75. Pfeiffer, B. E. & Foster, D. J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74–79 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Nobre, A. C. & Mesulam, M. M. in The Oxford Handbook of Attention (eds Nobre, A. C. & Kastner, S.) 105–151 (Oxford Univ. Press, 2014).

    Google Scholar 

  77. van Elswijk, G., Kleine, B. U., Overeem, S. & Stegeman, D. F. Expectancy induces dynamic modulation of corticospinal excitability. J. Cogn. Neurosci. 19, 121–131 (2007).

    PubMed  Google Scholar 

  78. Walter, W. G., Cooper, R., Aldridge, V. J., McCallum, W. C. & Winter, A. L. Contingent negative variation: an electric sign of sensori-motor association and expectancy in the human brain. Nature 203, 380–384 (1964).

    CAS  PubMed  Google Scholar 

  79. Los, S. A. & Heslenfeld, D. J. Intentional and unintentional contributions to nonspecific preparation. J. Exp. Psychol. Gen. 134, 52–72 (2005).

    PubMed  Google Scholar 

  80. Zanto, T. P. et al. Age-related changes in orienting attention in time. J. Neurosci. 31, 12461–12470 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Breska, A. & Deouell, L. Y. When synchronizing to rhythms is not a good thing: modulations of preparatory and post-target neural activity when shifting attention away from on-beat times of a distracting rhythm. J. Neurosci. 36, 7154–7166 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Mento, G., Tarantino, V., Sarlo, M. & Bisiacchi, P. S. Automatic temporal expectancy: a high-density event-related potential study. PLoS ONE 8, e62896 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Lima, B., Singer, W. & Neuenschwander, S. Gamma responses correlate with temporal expectation in monkey primary visual cortex. J. Neurosci. 31, 15919–15931 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Sharma, J. et al. Spatial attention and temporal expectation under timed uncertainty predictably modulate neuronal responses in monkey V1. Cereb. Cortex 25, 2894–2906 (2014).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  87. Jensen, O. & Mazaheri, A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci. 4, 186–194 (2010).

    PubMed  PubMed Central  Google Scholar 

  88. Jenkinson, N. & Brown, P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 34, 611–618 (2011).

    CAS  PubMed  Google Scholar 

  89. van Ede, F., de Lange, F., Jensen, O. & Maris, E. Orienting attention to an upcoming tactile event involves a spatially and temporally specific modulation of sensorimotor alpha-and beta-band oscillations. J. Neurosci. 31, 2016–2024 (2011). This is a study in humans that shows that modulation of alpha and beta oscillations by spatial attention is dynamically upregulated and downregulated by concurrent temporal expectations.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Rohenkohl, G. & Nobre, A. C. Alpha oscillations related to anticipatory attention follow temporal expectations. J. Neurosci. 31, 14076–14084 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Mathewson, K. E. et al. Making waves in the stream of consciousness: entraining oscillations in EEG alpha and fluctuations in visual awareness with rhythmic visual stimulation. J. Cogn. Neurosci. 24, 2321–2333 (2012).

    PubMed  Google Scholar 

  92. Samaha, J., Bauer, P., Cimaroli, S. & Postle, B. R. Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction. Proc. Natl Acad. Sci. USA 112, 8439–8444 (2015).

    CAS  PubMed  Google Scholar 

  93. Bonnefond, M. & Jensen, O. Alpha oscillations serve to protect working memory maintenance against anticipated distracters. Curr. Biol. 22, 1969–1974 (2012).

    CAS  PubMed  Google Scholar 

  94. van Diepen, R. M., Cohen, M. X., Denys, D. & Mazaheri, A. Attention and temporal expectations modulate power, not phase, of ongoing alpha oscillations. J. Cogn. Neurosci. 27, 1573–1586 (2015).

    PubMed  Google Scholar 

  95. Frohlich, F. & McCormick, D. A. Endogenous electric fields may guide neocortical network activity. Neuron 67, 129–143 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Schroeder, C. E. & Lakatos, P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 1, 9–18 (2009).

    Google Scholar 

  97. Lampl, I. & Yarom, Y. Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. J. Neurophysiol. 70, 2181–2186 (1993).

    CAS  PubMed  Google Scholar 

  98. Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I. & Schroeder, C. E. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110–113 (2008). This is a study in NHPs that introduces phase alignment of low-frequency oscillations with predictable rhythmic stimulation (entrainment) as a putative mechanism for selective temporal attention in the context of rhythmic stimuli.

    CAS  PubMed  Google Scholar 

  99. Stefanics, G. et al. Phase entrainment of human delta oscillations can mediate the effects of expectation on reaction speed. J. Neurosci. 30, 13578–13585 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Henry, M. J., Herrmann, B. & Obleser, J. Entrained neural oscillations in multiple frequency bands comodulate behavior. Proc. Natl Acad. Sci. USA 111, 14935–14940 (2014).

    CAS  PubMed  Google Scholar 

  101. Breska, A. & Deouell, L. Y. Neural mechanisms of rhythm-based temporal prediction: delta phase-locking reflects temporal predictability but not rhythmic entrainment. PLoS Biol. 15, e2001665 (2017).

    PubMed  PubMed Central  Google Scholar 

  102. Lakatos, P. et al. The spectrotemporal filter mechanism of auditory selective attention. Neuron 77, 750–761 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. ten Oever, S. et al. Low-frequency cortical oscillations entrain to subthreshold rhythmic auditory stimuli. J. Neurosci. 37, 4903–4912 (2017).

    PubMed  PubMed Central  Google Scholar 

  104. Shuler, M. G. H. Timing in the visual cortex and its investigation. Curr. Opin. Behav. Sci. 8, 73–77 (2016).

    PubMed  PubMed Central  Google Scholar 

  105. Doherty, J. R., Rao, A., Mesulam, M. M. & Nobre, A. C. Synergistic effect of combined temporal and spatial expectations on visual attention. J. Neurosci. 25, 8259–8266 (2005). This is a study in humans that reveals a synergistic interaction between temporal and spatial expectations in enhancing early visual evoked potentials.

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Ford, J. M. & Hillyard, S. A. Event-related potentials (ERPs) to interruptions of a steady rhythm. Psychophysiology 18, 322–330 (1981).

    CAS  PubMed  Google Scholar 

  107. Kujala, T., Kallio, J., Tervaniemi, M. & Naatanen, R. The mismatch negativity as an index of temporal processing in audition. Clin. Neurophysiol. 112, 1712–1719 (2001).

    CAS  PubMed  Google Scholar 

  108. Nordby, H., Roth, W. T. & Pfefferbaum, A. Event-related potentials to time-deviant and pitch-deviant tones. Psychophysiology 25, 249–261 (1988).

    CAS  PubMed  Google Scholar 

  109. Garcia, J. O., Srinivasan, R. & Serences, J. T. Near-real-time feature-selective modulations in human cortex. Curr. Biol. 23, 515–522 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. van Ede, F., Chekroud, S. R., Stokes, M. G. & Nobre, A. C. Decoding the influence of anticipatory states on visual perception in the presence of temporal distractors. bioRxiv http://dx.doi.org/10.1101/143123 (2017).

  111. Maunsell, J. H. R. & Treue, S. Feature-based attention in visual cortex. Trends Neurosci. 29, 317–322 (2006).

    CAS  PubMed  Google Scholar 

  112. Andersen, S. K., Fuchs, S. & Muller, M. M. Effects of feature-selective and spatial attention at different stages of visual processing. J. Cogn. Neurosci. 23, 238–246 (2011).

    PubMed  Google Scholar 

  113. White, A. L., Rolfs, M. & Carrasco, M. Stimulus competition mediates the joint effects of spatial and feature-based attention. J. Vis. 15, 7 (2015).

    PubMed  PubMed Central  Google Scholar 

  114. Treue, S. & Trujillo, J. C. M. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999).

    CAS  PubMed  Google Scholar 

  115. Cohen, M. R. & Maunsell, J. H. R. Using neuronal populations to study the mechanisms underlying spatial and feature attention. Neuron 70, 1192–1204 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Rohenkohl, G., Gould, I. C., Pessoa, J. & Nobre, A. C. Combining spatial and temporal expectations to improve visual perception. J. Vis. 14, 8 (2014).

    PubMed  PubMed Central  Google Scholar 

  117. Morillon, B., Schroeder, C. E., Wyart, V. & Arnal, L. H. Temporal prediction in lieu of periodic stimulation. J. Neurosci. 36, 2342–2347 (2016). This study in humans suggests distinct mechanisms for behavioural facilitation by different types of predictable temporal structures and demonstrates synergistic interactions between temporal and feature-based expectations.

    PubMed  PubMed Central  Google Scholar 

  118. SanMiguel, I., Widmann, A., Bendixen, A., Trujillo-Barreto, N. & Schröger, E. Hearing silences: human auditory processing relies on preactivation of sound-specific brain activity patterns. J. Neurosci. 33, 8633–8639 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Warren, S. G., Yacoub, E. & Ghose, G. M. Featural and temporal attention selectively enhance task-appropriate representations in human primary visual cortex. Nat. Commun. 5, 5643 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Astheimer, L. B. & Sanders, L. D. Listeners modulate temporally selective attention during natural speech processing. Biol. Psychol. 80, 23–34 (2009).

    PubMed  Google Scholar 

  121. Kotz, S. A., Schwartze, M. & Schmidt-Kassow, M. Non-motor basal ganglia functions: a review and proposal for a model of sensory predictability in auditory language perception. Cortex 45, 982–990 (2009).

    PubMed  Google Scholar 

  122. Nozaradan, S., Peretz, I., Missal, M. & Mouraux, A. Tagging the neuronal entrainment to beat and meter. J. Neurosci. 31, 10234–10240 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Tillmann, B. Music and language perception: expectations, structural integration, and cognitive sequencing. Top. Cogn. Sci. 4, 568–584 (2012).

    PubMed  Google Scholar 

  124. Lee, H. & Noppeney, U. Temporal prediction errors in visual and auditory cortices. Curr. Biol. 24, R309–R310 (2014).

    CAS  PubMed  Google Scholar 

  125. Kotz, S. A., Brown, R. M. & Schwartze, M. Cortico-striatal circuits and the timing of action and perception. Curr. Opin. Behav. Sci. 8, 42–45 (2016).

    Google Scholar 

  126. Naccache, L., Blandin, E. & Dehaene, S. Unconscious masked priming depends on temporal attention. Psychol. Sci. 13, 416–424 (2002).

    PubMed  Google Scholar 

  127. Martens, S. & Johnson, A. Timing attention: cuing target onset interval attenuates the attentional blink. Mem. Cogn. 33, 234–240 (2005).

    Google Scholar 

  128. Shen, D. & Alain, C. Implicit temporal expectation attenuates auditory attentional blink. PLoS ONE 7, e36031 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Hollerman, J. R. & Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304–309 (1998).

    CAS  PubMed  Google Scholar 

  130. Shuler, M. G. & Bear, M. F. Reward timing in the primary visual cortex. Science 311, 1606–1609 (2006). This is a study in rodents that demonstrates that neurons in the primary visual cortex are sensitive to temporal expectations about non-visual food rewards.

    CAS  PubMed  Google Scholar 

  131. Wilsch, A., Henry, M. J., Herrmann, B., Maess, B. & Obleser, J. Alpha oscillatory dynamics index temporal expectation benefits in working memory. Cereb. Cortex 25, 1938–1946 (2014).

    PubMed  Google Scholar 

  132. Thavabalasingam, S., O'Neil, E. B., Zeng, Z. & Lee, A. C. Recognition memory is improved by a structured temporal framework during encoding. Front. Psychol. 6, 2062–2062 (2015).

    PubMed  Google Scholar 

  133. Myers, N. E. et al. Testing sensory evidence against mnemonic templates. eLife 4, e09000 (2015).

    PubMed  PubMed Central  Google Scholar 

  134. van Ede, F., Niklaus, M. & Nobre, A. C. Temporal expectations guide dynamic prioritization in visual working memory through attenuated α oscillations. J. Neurosci. 37, 437–445 (2017). This recent study in humans demonstrates that temporal expectations operate within working memory, guiding temporally selective prioritization of mnemonic items when they are expected to become relevant for behaviour.

    CAS  PubMed  PubMed Central  Google Scholar 

  135. de Vries, I. E. J., van Driel, J. & Olivers, C. N. L. Posterior α EEG dynamics dissociate current from future goals in working memory-guided visual search. J. Neurosci. 37, 1591–1603 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Summerfield, C. & Egner, T. Expectation (and attention) in visual cognition. Trends Cogn. Sci. 13, 403–409 (2009).

    PubMed  Google Scholar 

  137. Friston, K. & Kiebel, S. Predictive coding under the free-energy principle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1211–1221 (2009).

    PubMed  PubMed Central  Google Scholar 

  138. Rescorla, R. A. & Wagner, A. R. in Classsical Conditioning II: Current Research and Theory (eds Black, A. H. & Prokasy, W. F.) 64–99 (New York: Appleton-Century Crofts, 1972).

    Google Scholar 

  139. Nobre, A. C. & Kastner, S. in The Oxford Handbook of Attention (eds Nobre, A. C. & Kastner, S.) 1201–1222 (Oxford Univ. Press, 2014).

    Google Scholar 

  140. Broadbent, D. E. & Broadbent, M. H. P. From detection to identification: response to multiple targets in rapid serial visual presentation. Percept. Psychophys. 42, 105–113 (1987).

    CAS  PubMed  Google Scholar 

  141. Raymond, J. E., Shapiro, K. L. & Arnell, K. M. Temporary suppression of visual processing in an RSVP task. J. Exp. Psychol. Hum. Percept. Perform. 18, 849–860 (1992).

    CAS  PubMed  Google Scholar 

  142. Kanwisher, N. G. Repetition blindness: type recognition without token individuation. Cognition 27, 117–143 (1987).

    CAS  PubMed  Google Scholar 

  143. Pashler, H. Dual–task interference in simple tasks. Psychol. Bull. 116, 220–244 (1994).

    CAS  PubMed  Google Scholar 

  144. Kleinfeld, D., Ahissar, E. & Diamond, M. E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 4, 435–444 (2006).

    Google Scholar 

  145. Schroeder, C. E., Wilson, D. A., Radman, T., Scharfman, H. & Lakatos, P. Dynamics of active sensing and perceptual selection. Curr. Opin. Neurobiol. 2, 172–176 (2010).

    Google Scholar 

  146. Bosman, C. A., Womelsdorf, T., Desimone, R. & Fries, P. A microsaccadic rhythm modulates gamma-band synchronization and behavior. J. Neurosci. 29, 9471–9480 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Harter, M. R. Excitability cycles and cortical scanning. Psychol. Bull. 68, 47–58 (1967).

    CAS  PubMed  Google Scholar 

  148. VanRullen, R. Perceptual cycles. Trends Cogn. Sci. 20, 723–735 (2016).

    PubMed  Google Scholar 

  149. Busch, N. A., Dubois, J. & VanRullen, R. The phase of ongoing EEG oscillations predicts visual perception. J. Neurosci. 29, 7869–7876 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M. & Ro, T. To see or not to see: prestimulus α phase predicts visual awareness. J. Neurosci. 29, 2725–2732 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Landau, A. N. & Fries, P. Attention samples stimuli rhythmically. Curr. Biol. 22, 1000–1004 (2012).

    CAS  PubMed  Google Scholar 

  152. 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).

    CAS  PubMed  Google Scholar 

  153. Tomassini, A., Spinelli, D., Jacono, M., Sandini, G. & Morrone, M. C. Rhythmic oscillations of visual contrast sensitivity synchronized with action. J. Neurosci. 35, 7019–7029 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Herbst, S. K. & Landau, A. N. Rhythms for cognition: the case of temporal processing. Curr. Opin. Behav. Sci. 8, 85–93 (2016).

    Google Scholar 

  155. Coull, J. T., Nobre, A. C. & Frith, C. D. The noradrenergic α2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting. Cereb. Cortex 11, 73–84 (2001).

    CAS  PubMed  Google Scholar 

  156. Parsons, B. D. et al. Lengthened temporal integration in schizophrenia. Neuropsychologia 51, 372–376 (2013).

    PubMed  Google Scholar 

  157. Cunnington, R., Iansek, R., Bradshaw, J. L. & Phillips, J. G. Movement-related potentials in Parkinson's disease: presence and predictability of temporal and spatial cues. Brain 118, 935–950 (1995).

    PubMed  Google Scholar 

  158. te Woerd, E. S., Oostenveld, R., de Lange, F. P. & Praamstra, P. A shift from prospective to reactive modulation of beta-band oscillations in Parkinson's disease. NeuroImage 100, 507–519 (2014).

    PubMed  Google Scholar 

  159. Hasler, R. et al. Attention-related EEG markers in adult ADHD. Neuropsychologia 87, 120–133 (2016).

    PubMed  Google Scholar 

  160. Dankner, Y., Shalev, L., Carrasco, M. & Yuval-Greenberg, S. Prestimulus inhibition of saccades in adults with and without attention-deficit/hyperactivity disorder as an index of temporal expectations. Psychol. Sci. 28, 835–850 (2017).

    PubMed  Google Scholar 

  161. Ivry, R. B. & Keele, S. W. Timing functions of the cerebellum. J. Cogn. Neurosci. 1, 136–152 (1989).

    CAS  PubMed  Google Scholar 

  162. O'Reilly, J. X., Mesulam, M. M. & Nobre, A. C. The cerebellum predicts the timing of perceptual events. J. Neurosci. 28, 2252–2260 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Avanzino, L. et al. The cerebellum predicts the temporal consequences of observed motor acts. PLoS ONE 10, e0116607 (2015).

    PubMed  PubMed Central  Google Scholar 

  164. Nombela, C., Hughes, L. E., Owen, A. M. & Grahn, J. A. Into the groove: can rhythm influence Parkinson's disease? Neurosci. Biobehav. Rev. 37, 2564–2570 (2013).

    PubMed  Google Scholar 

  165. Andrews, C. et al. Phase II trial of a syllable-timed speech treatment for school-age children who stutter. J. Fluency Disord. 48, 44–55 (2016).

    PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge support from a Wellcome Trust Senior Investigator Award (A.C.N.) (104571/Z/14/Z), a Marie Skłodowska-Curie Individual Fellowship from the European Commission (F.v.E.) (grant code ACCESS2WM) and the UK National Institute for Health Research (NIHR) Oxford Health Biomedical Research Centre. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust (203139/Z/16/Z). The authors also wish to thank K. Nussenbaum, A. Cravo, R. Auksztulewicz, S. Heideman and N. Myers for their thoughtful comments in the course of preparing this review, as well as A. Irvine and A. Board for their help with the bibliography. The authors also thank the reviewers for excellent constructive comments.

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A.C.N. and F.v.E. researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and/or edited the manuscript before submission.

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Correspondence to Anna C. Nobre.

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PowerPoint slides

Glossary

Temporal structures

Any repeating sets of intervals among two or more items.

Selective attention

The set of functions that prioritize and select relevant information to guide adaptive behaviour.

Receptive field

(RF). The aspect of the sensory environment to which a neuron is responsive — for example, a spatial location or a stimulus feature such as auditory pitch or visual orientation.

Temporal expectation

The state of the cognitive or neural system associated with the predicted timing of an event. The term has no implications concerning volition, awareness or conscious deliberation.

Predictive coding

A theoretical framework in which perceptual inferences are based on the difference between predicted and observed sensory inputs.

Learning theory

A theoretical framework for how learning is shaped by associations between stimuli or between actions and rewards. In reinforcement learning, for example, a key principle is that learning is driven by prediction errors (the differences in value between predicted and observed rewards).

Posner's spatial orienting task

An influential spatial attention task developed by Posner in which symbolic cues inform the most probable location of a future target stimulus.

Isochronous

Of a temporal structure with a constant inter-element interval; a regular beat.

Ordinal sequence

The order of elements that make up a sequence. For example, in SRT tasks, this refers to the order of the spatially arranged items to which participants must respond.

Temporal sequence

The timings between elements that make up a sequence.

Interval-time range

Cognitively relevant time range that ranges from several hundreds of milliseconds to several seconds.

Temporal updating

Updating of cognitive variables — such as expectations, the allocation of attention or movement plans — on the basis of estimates of elapsed time.

Evidence accumulation

The build-up of evidence for one of multiple perceptual decisions. In the literature on perceptual decision making, this is often studied using perceptual streams in which individual samples are insufficiently reliable, thus necessitating the integration of perceptual evidence over time.

Trace conditioning

A variation of classical conditioning in which the conditioned stimulus (such as a tone) and unconditioned stimulus (for example, an air puff) are separated by an empty time interval of a given duration.

Motor potential

Change in voltage associated with activity recorded from the muscle (electromyogram) upon stimulating the corresponding area of the primary motor cortex.

Event-related potentials

(ERPs). The average electrophysiological responses that are locked in time to a particular event of interest, such as a stimulus, action or other physiological marker.

Contingent negative variation

(CNV). A negative potential broadly distributed over the scalp that builds up before a target stimulus. Its intracranial sources include brain areas linked to motor preparation.

Phase

A point in an oscillatory period between 0 and 2π, corresponding to trough, rising slope, peak and so on.

P1 visual potential

A stereotypical event-related potential response that is characterized by a positive deflection in posterior sites approximately 100 ms after a visual input.

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Nobre, A., van Ede, F. Anticipated moments: temporal structure in attention. Nat Rev Neurosci 19, 34–48 (2018). https://doi.org/10.1038/nrn.2017.141

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