Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging

doi:10.1016/S0959-4388(03)00036-9

Current Opinion in Neurobiology

Volume 13, Issue 2, April 2003, Pages 250-255

https://doi.org/10.1016/S0959-4388(03)00036-9 Get rights and content

Abstract

A recent review of neuroimaging data on time measurement argued that the brain activity seen in association with timing is not influenced by specific characteristics of the task performed. In contrast, we argue that careful analysis of this literature provides evidence for separate neural timing systems associated with opposing task characteristics. The ‘automatic’ system draws mainly upon motor circuits and the ‘cognitively controlled’ system depends upon prefrontal and parietal regions.

Introduction

Every action we take and every stimulus we perceive has a temporal dimension. The neural mechanisms used to measure time are currently a topic of intensive investigation – the number of neuroimaging studies seeking to define and describe them is growing rapidly, including more than 20 studies published since the year 2000. To date, no strong consensus has been reached about which brain regions are involved in time measurement; however, a recent review [1^••] argues that the specific characteristics of the performed timing task do not affect the observed pattern of brain activity. Contrary to this, we suggest that much of the current ambiguity on the topic of neural time presentation may be due to the inappropriate grouping of studies that use very different time measurement tasks, thus drawing upon distinct neural timing systems. If this is the case, it should be possible to isolate the various neural systems involved in time measurement by a careful grouping of the literature, on the basis of the different task parameters used. In this review, we use precisely that approach, dividing studies of time representation according to three general task characteristics: the duration measured, the use of movement to define a temporal estimate, and the continuity and predictability of the task.

Section snippets

The importance of stimulus characteristics

Our decision to characterise studies in relation to interval duration and to use of movement builds on previous suggestions that these factors discriminate between two or more different time measurement systems. Evidence suggesting the existence of different neural systems for timing at different duration ranges includes: distinct psychophysical characteristics at different durations [2]; differential responses to pharmacological agents 2., 3., 4., 5., 6.; differential impairment of performance

The hypothesis: automatic versus cognitively controlled timing

On the basis of our predictions regarding how the three task characteristics discussed above draw on different neural resources, we propose that two distinct systems exist for measuring time in the types of behavioural tasks examined here. We also submit that each of the task characteristics discussed above helps to partially determine which system is active in any given task. One hypothesised system, which we will designate the ‘automatic’ timing system, is primarily involved in the continuous

Neuroimaging studies

Figure 1 summarises the published neuroimaging literature on primate time measurement 1.••, 9., 14., 27., 28., 29., 30., 31., 32., 33., 34., 35., 36., 37., 38., 39., 40., 41., 42., 43., 44., 45., 46., 47.••, 48., 49., 50., 51., 52.. It lists the areas of brain activity reported in each study in response to time measurement tasks. Tasks are categorised according to whether or not a duration greater than one second was measured, whether measured intervals were defined by movement, and whether

Challenges to the hypothesis — confounds

Because our analysis uses the most inclusive contrast from each dataset examined, much of the activity we describe may be due to task-related but non-temporal processes. Auditory, visual, and primary sensorimotor cortical activity found in association with automatic timing, for instance, might simply be due to sensory stimuli and motor responses. Some regions of the motor system, however, are active even in studies where very little movement or movement preparation (and in some cases none at

Conclusions

A clear dissociation in brain activity related to timing is seen when neuroimaging studies of time measurement are divided according the interval to be measured, the use of movement to define time, and the continuity or predictability of the task. This dissociation cannot be explained by confounding task characteristics alone, and thus provides support for the existence of two distinct systems for time measurement. One, which we term the ‘automatic’ system, is closely linked to the motor and

References and recommended reading

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

•
of special interest
••
of outstanding interest

Acknowledgements

This work was supported by the Wellcome Trust and the Medical Research Council, UK.

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Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging

Abstract

Introduction

Section snippets

The importance of stimulus characteristics

The hypothesis: automatic versus cognitively controlled timing

Neuroimaging studies

Challenges to the hypothesis — confounds

Conclusions

References and recommended reading

Acknowledgements

Act Nerv. Super (Praha)

Q. J. Exp. Psychol. B

Neuroimage

J. Physiol. (Lond)

Curr. Opin. Neurobiol.

J. Neurophysiol.

J. Neurosci.

J. Neurosci.

Psychol. Rev.

Exp. Brain Res.

Neuroreport

Neuropsychol.

Neuroreport.

J. Neurophysiol.

Exp. Brain Res.

Neuroimage

J. Cogn. Neurosci.

J. Neurosci.

Cereb. Cortex

Neuroreport

Activation of the supplementary motor area and of attentional networks during temporal processing

Exp. Brain Res.

Toward a neurobiology of temporal cognition: advances and challenges

Curr. Opin. Neurobiol.

Pharmacologic properties of the internal clock underlying time perception in humans

Neuropsychobiology

On dopaminergic modulation of temporal information processing

Biol. Psychol.

Duration discrimination of filled and empty auditory intervals: cognitive and perceptual factors

Percept. Psychophys.

The representation of temporal information in perception and motor control

Curr. Opin. Neurobiol.

Messages conveyed by spinocerebellar pathways during scratching in the cat. I. Activity of neurons of the lateral reticular nucleus

Brain Res.

Brain activity during non-automatic motor production of discrete multi-second intervals

Neuroreport