Neurophysiology of implicit timing in serial choice reaction-time performance

Abstract

Neural representations of time for the judgment of temporal durations are reflected in electroencephalographic (EEG) slow brain potentials, as established in time production and perception tasks. Here, we investigated whether anticipatory processes in reaction-time procedures are governed by similar mechanisms of interval timing. We used a choice reaction task with two different, temporally regular stimulus presentation regimes, both with occasional deviant interstimulus intervals. Temporal preparation was shown in the form of adjustments in time course of slow brain potentials, such that they reached their maximum amplitude just before a new trial, independent of the duration of the interstimulus interval. Preparation was focused on a brief time window, demonstrated by a drop in amplitude of slow potentials as the standard interval had elapsed in deviant interstimulus intervals. Implicit timing influencing perceptual processing was shown in reduced visual-evoked responses to delayed stimuli after a deviant interstimulus interval and in a reduction of EEG alpha power over the visual cortex at the time when the standard interval had elapsed. In contrast to explicit timing tasks, the slow brain potential manifestations of implicit timing originated in the lateral instead of the medial premotor cortex. Together, the results show that temporal regularities set up a narrow time window of motor and sensory attention, demonstrating the operation of interval timing in reaction time performance. The divergence in slow brain potential distribution between implicit and explicit timing tasks suggests that interval timing for different behaviors relies on qualitatively similar mechanisms implemented in distinct cortical substrates.

Figure 1.

Schematic of the long and short SOA trial sequences. Stimuli were presented in short series of 11, 13, 15, 17, 19, or 21 trials. Each series of stimuli had SOAs of either 1.5 or 2.0 s, except for the last SOA, which was always 1.75 s.

Figure 2.

Scalp topography and CNV waveforms in short and long SOA conditions separately for left (top) and right (bottom) response blocks. Waveforms represent averaged activity of four electrodes overlying the left (PM-L) and right (PM-R) premotor cortex activation maxima. Line spacing in the scalp maps is 0.5 μV. The dashed lines indicate the 1500 and 2000 ms SOA durations.

Figure 3.

Effect of timing perturbation on slow brain potentials. The topography of the CNV in the long deviant condition (1400–1500 ms) is similar to the topography seen with regular SOA. The CNV over left and right premotor areas peaks at ∼1600 ms (i.e., shortly after the expected time of stimulus arrival) and drops in amplitude before stimulus presentation at 1750 ms (arrow heads). The dashed lines indicate the expected 1500 and 2000 ms SOA durations. In the top traces, a regression line is fitted to the downgoing slope of the CNV in the long deviant condition. Line spacing in the scalp maps is 0.5 μV.

Figure 4.

β-Band (14–24 Hz) modulation in precentral cortex. The graphs show β-power change relative to baseline in time windows of 850–1150 ms (early) and 1150–1450 ms (late). The grand average beamformer estimate of the β-power change in the long SOA condition with right-hand response (window 850–1150 ms) is shown. Error bars indicate SEM.

Figure 5.

Modulation of visual evoked potentials and α activity. TSE traces represent the temporal evolution of α activity during the deviant final SOAs of 1750 ms (time indicated by arrowheads). α Activity decreases sharply at 1500 ms (i.e., the time of the expected stimulus) in the short SOA condition. α Activity continues unchanged when the stimulus is expected at 2000 ms. The difference is quantified between 1650 and 1850 ms (gray bar) and represented in a t map showing a distribution over the occipital scalp (uncorrected, two-tailed t test). The four gray shades represent t values between 2.2 and 4.0 (critical t value for p < 0.05: 2.26). The stimulus in the long deviant condition occurring later than anticipated evoked a visual response of reduced amplitude, as illustrated in the ERP traces from four pooled electrodes. For better visualization, the visual-evoked responses are low-pass filtered (10 Hz) and displayed and quantified relative to a baseline between 1500 and 1750 ms.

Figure 6.

Minimum norm current estimates of the CNV (left) and movement-related activity (right). The current estimate for the CNV refers to a time point 200 ms before the reaction stimulus. The movement-related sources were estimated at peak latency 40 ms before the button press. The source locations of the movement-related activity serve as landmarks for verification of the origin of the frontal CNV maxima.