Cingulate activation increases dynamically with response speed under stimulus unpredictability

Abstract

Functional magnetic resonance imaging studies of cognition require repeated and consistent engagement of the cognitive process under investigation. Activation is generally averaged across trials that are assumed to tax a specific mental operation or state, whereas intraindividual variability in performance between trials is usually considered error variance. A more recent analysis approach postulates that these fluctuations can reflect variation in the very process taxed by the particular trial type. In the present study, participants responded to targets presented randomly in 1 of 4 peripheral locations. By employing a function of reaction time (RT) of individual trials as a linear regressor, brain regions were identified whose activation varied with RT on a trial-by-trial basis. Whole-brain analysis revealed that the anterior cingulate, posterior cingulate, and left angular/superior temporal gyri were more active in trials with faster RT but only when the target location was unpredictable. No such association was seen in trials where the target location was predicted by a central cue. These results suggest a role for the cingulate and angular gyri in the dynamic regulation of attention to unpredictable events. This is in accordance with the function of a default network that is active in the absence of top-down-focused attention and is thought to continuously provide resources for broad and spontaneous information gathering. Exploiting intertrial performance variability may be particularly suitable for capturing such spontaneous and elusive phenomena as stimulus-driven processes of attention.

Figure 1

Components of a CUED and an UNCUED target trial in the Spatial Attentional Resource Allocation Task (SARAT). Onset of a central cue preceded target onset by a variable SOA of 400, 700, 1000 or 1300 ms. The target was presented for 500 ms in the continuing presence of the cue, which remained on display until 500 ms after target offset. Only screen background was then presented for an intertrial interval that varied in length such that total trial duration was always 2700 ms.

Figure 2

RT (mean ± SEM) differed with Stimulus Onset Asynchrony (SOA), and this effect depended on trial type (*P<0.05, **P<0.01, ***P<0.001, paired t-tests).

Figure 3

Brain regions whose activation in UNCUED trials increased with $\frac{1}{{\mathit{RT}}_i}$ on a trial-by-trial basis. Group activation maps are overlaid onto one anatomical scan in Talairach space. All three regions significantly increased in activation with faster responding in UNCUED but not in CUED trials. Activation is expressed as the percentage of change in the amplitude of activation per standard deviation (stdev) unit of change in $\frac{1}{{\mathit{RT}}_i}$.

Figure 4

Activation in the anterior and posterior cingulate and in the left angular gyrus plotted against $\frac{1}{{\mathit{RT}}_i}$ for CUED and UNCUED trials. Graphs are based upon measured beta weights. A significant positive association is observed in UNCUED but not in CUED trials.

Figure 5

Mean percentage of signal change in the anterior and posterior cingulate gyrus across trials. These values differed (*P<0.05) between CUED and UNCUED trials, but no condition displayed a significant overall activation or deactivation relative to baseline.