Brain activation patterns during measurement of sub- and supra-second intervals
Introduction
There are a number of reasons to believe that different systems are used to measure time at the milliseconds and multisecond ranges. The measurement of tens or hundreds of milliseconds is important for coordination of muscles during movement (Hore, Wild, & Diener, 1991), while the measurement of multisecond durations is more commonly associated with learned behaviours such as social interaction or foraging (Brunner, Kacelnik, & Gibbon, 1992; Pyke, Pulliam, & Charnov, 1977). Time measurement has also been shown to have quite different properties at these two duration ranges. For instance, psychophysical characteristics differ (Gibbon, Malapani, Dale, & Gallistel, 1997), pharmacological agents (Mitriani, Shekerdijiiski, Gourevitch, & Yanev, 1977; Rammsayer, 1999) and the distraction of attention in dual task scenarios (Rammsayer & Lima, 1991) can have differential influence (but see Macar, Grondin, & Casini, 1994), while lesions to specific brain areas elicit differential impairments (Clarke, Ivry, Grinband, Roberts, & Shimizu, 1996). Based on these observations, several authors (Gibbon et al., 1997, Hazeltine, 1997, Ivry, 1996; Lewis & Miall, 2003; Rammsayer, 1999) have hypothesised that time intervals in the millisecond and multisecond ranges are measured by independent brain mechanisms. Further, we have recently suggested (Lewis & Miall, 2003) that parts of the motor system may be involved in the automatic measurement of briefer durations, while flexible cognitive modules of the prefrontal and parietal cortex are recruited for the measurement of longer periods.
Neuroimaging studies of sub- and supra-second interval measurements frequently show disparate results, although some areas appear to be consistently activated by timing at both durations (see Lewis & Miall, 2003; Macar et al., 2002 for reviews). However the task paradigms used at these two ranges are normally quite different, making it impossible to determine whether disparities in result are linked to the duration of the measured interval or to other factors. We are aware of only one neuroimaging study to date which has presented separate results from timing of sub- and supra-second intervals using the same task (Rubia et al., 1998). Subjects tapped in synchrony with a visual cue which appeared either every 0.6 or every 5 s. Production of the longer interval activated a different network of areas than production of the shorter interval, with only the right hemispheric frontal pole and anterior cingulate commonly active during both. Because the authors did not perform a direct comparison between the datasets, however, we cannot say if the observed differences in pattern are significant. Furthermore, because no control was provided for sensorimotor activities, it is impossible to be certain whether the differences were related to timing, or to other factors such as movement and sensory perception. In another study (Macar et al., 2002) subjects reproduced intervals in two different supra-second ranges (2.2–3.2 and 9–13 s), showing a similar pattern of activity for both intervals. In a third study (Rao et al., 1997) subjects produced two different sub-second intervals, 300 and 600 ms, using auditory-paced finger tapping, with almost identical results for the two.
The goal of our current investigation was to search for differences in brain activity associated with measurement of intervals longer than 2 s and briefer than 1 s, driven by the hypothesis that different neural systems would be used for each interval range. For this purpose, we chose to examine 0.6 and 3 s. We hypothesise that timing of the shorter interval would preferentially activate cortical and cerebellar motor systems whereas timing of the longer interval would draw more heavily upon prefrontal and parietal cortices. Our design ensured that the same task was used for both intervals and controlled for any non-timing related confounds associated with the difference in duration by using a cognitive subtraction.
Section snippets
Subjects
Eight right-handed subjects gave written informed consent before participating. Mean age was 26 and three were female. The experiment was approved by the Central Oxfordshire Research Ethics Committee.
Task
We used a temporal discrimination task, with visual discrimination for control and repeated the complete experimental paradigm separately for each of the two different standard durations (0.6 and 3 s) with order of presentation randomised across subjects. The behavioural conditions were: TIME,
Behavioural performance
Because of the limited number of trials completed during fMRI data collection, the psychometric staircase was not perfectly stable. When tested at the 0.6 s interval, instead of the intended 85% correct, subjects achieved a mean accuracy of 83% correct (S.D. 4.5%) on the TIME task and 89% correct (S.D. 4.5%) on the LENGTH task, with the difference between these falling just short of significance (two-tailed paired t-test P=0.06). When tested at the 3 s interval where fewer trials were completed
Discussion
In this experiment, we examined the brain activity associated with measurement of 0.6 and 3 s intervals using a temporal discrimination task. We first analysed the results separately for each interval using the cognitive subtraction TIME–LENGTH to remove confounding activities due to stimulus presentation and subject responses, and next directly compared the results of this subtraction across the two intervals in order to determine the regions of activity which differed significantly between the
Acknowledgements
We thank Alex Kacelnik for his input in this work, and Richard Ivry for useful comments. RCM and PAL were supported by the Wellcome Trust and PAL by an Overseas Research Studentship. Additional support was provided by the MRC funded Oxford fMRIB Centre. We thank fMRIB staff for generous technical support and advice.
References (62)
- et al.
Pattern generation
Current Opinion in Neurobiology
(1997) - et al.
Messages conveyed by spinocerebellar pathways during scratching in the cat. Part I. Activity of neurons of the lateral reticular nucleus
Brain Research
(1978) - et al.
The neuroanatomical substrate of sound duration discrimination
Neuropsychologia
(2002) - et al.
Optimal foraging and timing processes in the starling, Sturnus vulgaris: Effect of inter-capture interval
Animal Behaviour
(1992) - et al.
Orienting attention in time: Behavioural and neuroanatomical distinction between exogenous and endogenous shifts
Neuropsychologia
(2000) - et al.
Microcircuitry and function of the inferior olive
Trends in Neurosciences
(1998) Anisotropies of perceived contrast and detection speed
Vision Research
(1982)- et al.
Toward a neurobiology of temporal cognition: Advances and challenges
Current Opinion in Neurobiology
(1997) - et al.
Neural network models of cortical functions based on the computational properties of the cerebral cortex
Journal of Physiology Paris
(1994) The representation of temporal information in perception and motor control
Current Opinion in Neurobiology
(1996)
Cerebellar timing systems
International Review of Neurobiology
Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists
Cognitive Brain Research
A global optimisation method for robust affine registration of brain images
Medical image analysis
The basic pattern of activation in motor and sensory temporal tasks: Positron emission tomography data
Neuroscience Letters
Brain activation induced by estimation of duration: A PET study
Neuroimage
Cortical networks recruited for time perception: A monkey positron emission tomography (PET) study
Neuroimage
Language within our grasp
Trends in Neurosciences
Working memory for location and time: Activity in prefrontal area 46 relates to selection rather than maintenance in memory
Neuroimage
Prefrontal involvement in “temporal bridging” and timing movement
Neuropsychologia
The functional organization of the lateral frontal cortex: Conjecture or conjuncture in the electrophysiology literature
Trends in Cognitive Sciences
Time perception and motor timing: A common cortical and subcortical basis revealed by fMRI
Neuroimage
Functional localization of a “Time Keeper” function separate from attentional resources and task strategy
Neuroimage
The supraspinal control of mammalian locomotion
Journal of Physiology
Effects of divided attention on temporal processing in patients with lesions of the cerebellum or frontal lobe
Neuropsychology
Where and when to pay attention: The neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI
Journal of Neuroscience
The roles of the cerebellum and basal ganglia in timing and error prediction
European Journal of Neuroscience
Cerebral correlates of working memory for temporal information
NeuroReport
Neural mechanisms of timing
Trends in Cognitive Sciences
Cerebellar dysmetria at the elbow, wrist, and fingers
Journal of Neurophysiology
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