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The neural bases for timing of durations

Abstract

Durations are defined by a beginning and an end, and a major distinction is drawn between durations that start in the present and end in the future (‘prospective timing’) and durations that start in the past and end either in the past or the present (‘retrospective timing’). Different psychological processes are thought to be engaged in each of these cases. The former is thought to engage a clock-like mechanism that accurately tracks the continuing passage of time, whereas the latter is thought to engage a reconstructive process that utilizes both temporal and non-temporal information from the memory of past events. We propose that, from a biological perspective, these two forms of duration estimation are supported by computational processes that are both reliant on population state dynamics but are nevertheless distinct. Prospective timing is effectively carried out in a single step where the ongoing dynamics of population activity directly serve as the computation of duration, whereas retrospective timing is carried out in two steps: the initial generation of population state dynamics through the process of event segmentation and the subsequent computation of duration utilizing the memory of those dynamics.

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Fig. 1: Prospective and retrospective timing.
Fig. 2: Neural trajectories during prospective timing.
Fig. 3: Single-cell activity underlying stable neural trajectories during prospective timing.
Fig. 4: Neural event trajectories encode event structure of experience.
Fig. 5: Relation between duration estimates and event trajectories.

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Acknowledgements

The authors dedicate this Review to the memory of Warren H. Meck. Sadly, Warren passed away in 2020 before they could complete the writing of this Review. However, it was first proposed by him as an opportunity to bring together two fields of time research which have long been isolated from each other, and the authors are honoured and grateful to continue this work in his memory. The authors thank V. van Wassenhove for discussion and comments on the manuscript. The work was supported by a Synergy Grant from the European Research Council to E.I.M. (‘KILONEURONS’, grant agreement number 951319), an RCN FRIPRO grant to E.I.M. (grant number 286225), a Centre of Excellence scheme grant to M.-B.M. and E.I.M. from the Research Council of Norway (Centre for Neural Computation, grant number 223262), the Kavli Foundation (M.-B.M. and E.I.M.), and a direct contribution to M.-B.M. and E.I.M. from the Ministry of Education and Research of Norway.

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Glossary

Prospective timing

The estimation of an ongoing duration in the present moment.

Events

The basic units of organization for experience, defined primarily as perceived time intervals whose beginnings and ends are clearly defined.

Retrospective timing

The estimation of duration based on memory of past events.

Population clock

The encoding of temporal information through changes in neural population activity over time.

Explicit timing

Prospective timing in which subjects are aware that they should attend to the passage of time to either estimate a duration defined by external events or generate a timed action.

Neural trajectory

A sequence of population states over time which describe the evolution of neural population activity.

Implicit timing

Prospective timing in which no overt timing behaviour is required.

Recurrent neural networks

Neural networks in which each unit can receive input from other units in the network in addition to external input.

Event segmentation

The parcellation of continuous ongoing experience into discrete events.

Event trajectory

A neural trajectory defined through the process of event segmentation.

Contextual drift

A dynamic in which representations of context gradually change over time, as a natural result of time-varying inputs.

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Tsao, A., Yousefzadeh, S.A., Meck, W.H. et al. The neural bases for timing of durations. Nat Rev Neurosci 23, 646–665 (2022). https://doi.org/10.1038/s41583-022-00623-3

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