Accumulation of neural activity in the posterior insula encodes the passage of time - PubMed (original) (raw)

Accumulation of neural activity in the posterior insula encodes the passage of time

Marc Wittmann et al. Neuropsychologia. 2010 Aug.

Abstract

A number of studies have examined the perception of time with durations ranging from milliseconds to a few seconds, however the neural basis of these processes are still poorly understood and the neural substrates underlying the perception of multiple-second intervals are unknown. Here we present evidence of neural systems activity in circumscribed areas of the human brain involved in the encoding of intervals with durations of 9 and 18s in a temporal reproduction task using event-related functional magnetic resonance imaging (fMRI). During the encoding there was greater activation in more posterior parts of the medial frontal and insular cortex whereas the reproduction phase involved more anterior parts of these brain structures. Intriguingly, activation curves over time show an accumulating pattern of neural activity, which peaks at the end of the interval within bilateral posterior insula and superior temporal cortex when individuals are presented with 9- and 18-s tone intervals. This is consistent with an accumulator-type activity, which encodes duration in the multiple seconds range. Given the close connection between the dorsal posterior insula and ascending internal body signals, we suggest that the accumulation of physiological changes in body states constitutes our experience of time. This is the first time that an accumulation function in the posterior insula is detected that might be correlated with the encoding of time intervals.

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Figures

Fig. 1

Fig. 1

Experimental Design. Trial events in the temporal reproduction and the control reaction time task: To discourage subjects from counting (which they were instructed not to), in both the timing and the control task, a secondary memory task had to be performed. In the timing task, subjects first saw for three seconds four numbers on the screen. Then, a continuous 1.2 Hz tone was presented for one of three durations (3-, 9-, 18-s). After the tone had stopped subjects had to press a button as fast as possible. After a short pause a continuous 2 Hz tone was presented that had to be stopped by pressing a button when the subjects thought that it has lasted as long as the first stimulus. Then one single number appeared on the screen and subjects had to decide by pressing one of two buttons whether it was one of the four numbers seen at the beginning of the trial. The control reaction time task was characterized by subjects reacting as fast as possible with a button press when a 1.2 Hz tone stopped.

Fig. 2

Fig. 2

Brain activity during the 9-s (left) and 18-s (right) encoding phase. A sagittal (x=8) and an axial slice (z=14) show significant brain activity (p < 0.01, corrected) in three regions encompassing a bilateral medial frontal area (SMA), left and right posterior insula (p Ins) as well as superior temporal cortex (ST) as related to the encoding versus control contrast in the 9-s and 18-s conditions. Individual time activity curves (set to zero at the onset of the stimulus) show an inverted u-shape function in the SMA and climbing brain activity that peaks at the end of the stimulus (with a delay of ca. 6 seconds reflecting the hemodynamic response function) for left (L) and right (R) p Ins, ST.

Fig. 3

Fig. 3

Brain activity during the 9-s and 18-s reproduction phase. A sagittal (x=4) and an axial slice (z=2) show significant brain activity (p < 0.01, corrected) in three regions encompassing right medial frontal areas (SMA, medial F), left and right anterior insula (a Ins) as well as inferior frontal cortex (IF) as related to the reproduction versus control contrast in the 9-s and 18-s conditions. Time activity curves in the ROI as registered during the reproduction phase, namely right SMA and bilateral anterior insula (a Ins) and inferior frontal (IF) cortex, peak just before the button press.

Fig. 4

Fig. 4

Significant brain activation for the contrast reproduction versus encoding phase (p < 0.01, corrected) on two axial (z = 2, 12) and one sagittal plane (x = 7). Stronger activation in the reproduction phase is colored in yellow to red (focus point: bilateral anterior insula, a Ins), stronger activation in the encoding phase is coded in blue (focus point: bilateral posterior insula, p Ins).

Fig. 5

Fig. 5

Brain activity related to the 9-s and 18-s control condition. Time activity curves registered in the ROI for the 9-s and 18-s encoding versus control conditions displayed for the control phase lasted on average 7.5 s and 12.7 s, respectively. No significant slopes are detected during this control duration phase.

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