Available online at www.sciencedirect.com Dissociating explicit timing from temporal expectation with fMRI JT Coull 1 and AC Nobre 2 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. Addresses 1 Laboratoire de Neurobiologie de la Cognition, Universite ´ de Provence & CNRS, Po ˆ le 3C, 3 Place Victor Hugo, 13331 Marseille Cedex 3, France 2 Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK Corresponding author: Coull, JT (jennifer.coull@univ-provence.fr) Current Opinion in Neurobiology 2008, 18:137–144 This review comes from a themed issue on Cognitive neuroscience Edited by Read Montague and John Assad Available online 12th August 2008 0959-4388/$ – see front matter # 2008 Elsevier Ltd. All rights reserved. DOI 10.1016/j.conb.2008.07.011 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 [6–8]? We attempt to resolve some of these puzzles by decon- structing 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 out- lined by Battelli [9]. Functional definitions: explicit versus implicit timing 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 timing’), in which subjects represent the timed duration or ISI with a sustained, delayed or periodic motor act (Figure 2b and c). In all cases, the ‘task goal’ for the subject is to provide an accurate estimate of elapsed time. Implicit timing Implicit timing, on the contrary, is engaged as a by- product of non-temporal task goals, when sensory stimuli or motor responses nevertheless adhere to a strict temporal framework. For example, task instructions may require subjects to make a perceptual judgement about stimulus features or to perform a specific motor act. Even though no overt estimates of stimulus or action duration are required, any temporal structure inherent in the rate of stimulus presentation or motor execution will engage timing mechanisms implicitly. For tasks in which implicit timing is indexed by the temporal regularity of a motor output timing is said to emerge as a by-product of the dynamics of motor control (‘emergent timing’) [10,11]. However, for tasks in which implicit timing is indexed by the temporal predictability of perceptual input timing is used to build an expectation of when the next stimulus will appear. Moreover, the implicit use of timing to establish temporal expectations may be subconscious and unintentional (‘exogenous’) or conscious and deliberate (‘endogenous’) (see Figure 1). Exogenous temporal expectations are engaged incidentally as the by-product of a temporally regular stimulus structure (Figure 3a). Endogenous www.sciencedirect.com Current Opinion in Neurobiology 2008, 18:137–144