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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.

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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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Contributions

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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