Dissociating explicit timing from temporal expectation with fMRI

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Explicit timing is engaged whenever subjects make a deliberate estimate of discrete duration in order to compare it with a previously memorised standard. Conversely, implicit timing is engaged, even without a specific instruction to time, whenever sensorimotor information is temporally structured and can be used to predict the duration of future events. Both emergent timing (motor) and temporal expectation (perceptual) are forms of implicit timing. Recent fMRI studies demonstrate discrete neural substrates for explicit and implicit timing. Specifically, basal ganglia are activated almost invariably by explicit timing, with co-activation of prefrontal, premotor and cerebellar areas being more context-dependent. Conversely, implicit perceptual timing (or “temporal expectation”) recruits cortical action circuits, comprising inferior parietal and premotor areas, highlighting its role in the optimisation of prospective behaviour.

Introduction

The cognitive neuroscience of interval timing (i.e. timing in the range of several hundred milliseconds to minutes) is plagued by several neuroanatomical dichotomies. Is there a left- or right-sided hemispheric lateralisation for timing [1, 2]? Are there anatomical differences in the processing of subsecond versus suprasecond durations [3, 4]? Do distinct neural systems subserve perceptual versus motor timing [4, 5]? More generally, is there one ubiquitous task-independent timing network, or is timing represented locally in functionally specific areas [6, 7, 8]? We attempt to resolve some of these puzzles by deconstructing the monolithic term ‘timing’ and making clear the functional (and neural) distinction between explicit and implicit timing of stimulus duration or inter-stimulus intervals (Figure 1). Our aim is to show that some of the apparent inconsistency, and consequent confusion, has arisen from a conflation of these processes. Specifically, we use results from the functional magnetic resonance imaging (fMRI) literature, highlighting those studies appearing within the past three years, to illustrate their discrete neural signatures. We restrict our discussion to metrical representations of time. The neural correlates of ordinal representations of time have recently been outlined by Battelli [9].

Section snippets

Explicit timing

The crucial distinction between explicit and implicit timing is whether or not the task instructions require subjects to provide an overt estimate of duration. In tasks of explicit timing, estimates of stimulus duration or inter-stimulus interval (ISI) are given either in the form of a perceptual discrimination (‘perceptual timing’), in which subjects typically state whether one stimulus duration or ISI is shorter or longer than another (Figure 2a); or in the form of a motor response (‘motor

Neuroanatomical substrates of explicit timing

Numerous fMRI studies of perceptual [16, 17, 18, 19, 20, 21, 22, 23, 24•] or motor [26, 27, 28, 29, 30, 31•, 32••, 33, 34] timing have consistently identified several key ‘timing areas’: supplementary motor area (SMA), basal ganglia (BG), cerebellum and right inferior frontal and parietal cortices. The functional contribution, or necessity, of each to a timing network is still very much a matter of debate however.

Neuroanatomical substrates of implicit timing: temporal expectations

We restrict our review to studies of implicit perceptual timing, or ‘temporal expectations’ (Figure 1), and refer the reader to Ivry et al. [40] for a discussion of implicit motor (‘emergent’) timing.

Responses to sensory stimuli that appear when expected are quicker and more accurate than those appearing at unexpected intervals [15]. Such temporal expectations (also referred to as implicit timing [14], anticipation of event timing [41, 42] or future-oriented attending [12]) make use of timing

Hemispheric lateralisation for explicit timing and temporal expectation

Recently, Geiser et al. [59••] have directly compared implicit perceptual timing (i.e. temporal expectation) with explicit timing of a verbal rhythm task. They identified a clear-cut hemispheric lateralisation, with right-sided temporo-parietal areas being activated by explicit timing of temporally predictable rhythmic speech patterns, while their left-sided homologues were activated by implicit temporal processing of the same stimuli. This experiment exemplifies, at least for perceptual timing

Conclusions

We aimed to imbue some clarity into the disparate findings in the timing literature by re-classifying it into those studies in which timing is the explicit task goal versus those in which timing is conducted implicitly in order to achieve a motor or perceptual goal. Explicit timing almost invariably engages BG, while activation of SMA, inferior frontal cortex and cerebellum, although common, depends more upon the specific task-context. Implicit perceptual timing activates a different set of

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgement

JTC is partly funded by a grant from the Agence Nationale de la Recherche, Programme 2007 Neurosciences, Neurologie & Psychiatrie.

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