Functional neural circuits for mental timekeeping

Abstract

Theories of mental timekeeping suggest frontostriatal networks may mediate performance of tasks requiring precise timing. We assessed whether frontostriatal networks are functionally integrated during the performance of timing tasks. Functional magnetic resonance imaging (fMRI) data from 31 healthy adults were collected during performance of several different types of discrete interval timing tasks. Independent component analysis (ICA) was used to examine functional connectivity within frontostriatal circuits. ICA identifies groups of spatially discrete brain regions sharing similar patterns of hemodynamic signal change over time. The results confirm the existence of a frontostriatal neural timing circuit that includes anterior cingulate gyrus, supplementary motor area, bilateral anterior insula, bilateral putamen/globus pallidus, bilateral thalamus, and right superior temporal gyrus and supramarginal gyrus. Several other distinct neural circuits were identified that may represent the neurobiological substrates of different information processing stages of mental timekeeping. Small areas of right cerebellum were engaged in several of these circuits, suggesting that cerebellar function may be important in, but not the primary substrate of, the mental timing tasks used in this experiment. These findings are discussed within the context of current biological and information processing models of neural timekeeping.

Figure 1

Illustration of eight independent components identified in the analysis. The overlay was constructed in ascending order of R² association with the experimental design, with the weakest component entered first. Because there is overlap of some brain regions across components, a detailed list of what brain areas comprise each component is listed in Table I, along with a color key identifying each. All component maps are thresholded at P < 0.000001 FWE, corrected for searching the whole brain.

Figure 2

Illustration of component 2 showing regions consistent with default mode network. Brain regions showing positive signal change during task performance are shown in red. Regions with true negative signal change are shown in blue. The cerebellum coronal rendering is depicted from the posterior view. Statistical results are thresholded at P < 0.00001 FWE, corrected for searching the whole brain. Time courses (right) for task and rate conditions depict average amplitude of the hemodynamic response for the ICA time course following start of task blocks (time 0), adjusted for other regressors in the experimental design.

Figure 3

Illustration of component 5 showing cortical regions that reduce hemodynamic activity during syncopation tasks (blue). Statistical results are thresholded at P < 0.00001 FWE, corrected for searching the whole brain. Time courses (right) for task conditions depict average amplitude of the hemodynamic response for the ICA time course following start of task blocks (time 0), adjusted for other regressors in the experimental design.

Figure 4

Illustration of component 7 showing a frontal‐parietal‐cerebellar network whose activity differs between the fastest and slowest rates of stimulus presentation. Brain regions showing positive signal change during task performance are shown in red‐yellow. Regions with negative signal change are shown in blue. The cerebellum coronal rendering is depicted from the posterior view. Statistical results are thresholded at P < 0.00001 FWE, corrected for searching the whole brain. Time courses (right) for rate conditions depict average amplitude of the hemodynamic response for the ICA time course following start of task blocks (time 0), adjusted for other regressors in the experimental design.