Flexible neural mechanisms of cognitive control within human prefrontal cortex

Abstract

A major challenge in research on executive control is to reveal its functional decomposition into underlying neural mechanisms. A typical assumption is that this decomposition occurs solely through anatomically based dissociations. Here we tested an alternative hypothesis that different cognitive control processes may be implemented within the same brain regions, with fractionation and dissociation occurring on the basis of temporal dynamics. Regions within lateral prefrontal cortex (PFC) were examined that, in a prior study, exhibited contrasting temporal dynamics between older and younger adults during performance of the AX-CPT cognitive control task. The temporal dynamics in younger adults fit a proactive control pattern (primarily cue-based activation), whereas in older adults a reactive control pattern was found (primarily probe-based activation). In the current study, we found that following a period of task-strategy training, these older adults exhibited a proactive shift within a subset of the PFC regions, normalizing their activity dynamics toward young adult patterns. Conversely, under conditions of penalty-based monetary incentives, the younger adults exhibited a reactive shift some of the same regions, altering their temporal dynamics toward the older adult baseline pattern. These experimentally induced crossover patterns of temporal dynamics provide strong support for dual modes of cognitive control that can be flexibly shifted within PFC regions, via modulation of neural responses to changing task conditions or behavioral goals.

Fig. 1.

(A) The set of 17 age-related crossover ROIs originally reported in ref. . (B) Activation dynamics during trial for younger and older adults (averaged across all ROIs). Older adults show reduced cue-related but increased probe-related activity, associated with a reactive control mode.

Fig. 2.

(A) The set of 4 regions demonstrating training-related proactive shift (increased cue-related activity, decreased probe-related activity) in older adults and penalty-related reactive shift (decreased cue-related activity, increased probe-related activity) in young adults. The right side of the image is the right side of the brain, and the left side of the image is the left side of the brain. The region in red is the left middle frontal gyrus (BA 9/46; x = −35, y = 44, z = 32); yellow is the medial superior frontal gyrus (BA 6; x = −46, y = −7, z = 41). Two right inferior frontal junction regions (BA 44/6) are in green (x = 39, y = 6, z = 33) and blue (x = 53, y = 6, z = 36). (B) Activation dynamics for older adults at baseline and posttest conditions in 4 regions identified in (A). (C) Activation dynamics for young adults at baseline and penalty conditions in 4 regions identified in (A). (D) Shift from sustained to primarily cue-related to primarily probe-related activation dynamics in right IFJ across reward, baseline and penalty AX-CPT conditions, respectively. Cue and probe activation computed by average of time points 3–4 (cue) and 5–6 (probe). Inset shows location of contiguous right IFJ regions showing penalty-related reactive pattern (blue) and reward-related sustained proactive pattern (red).