Developmental Dissociations in Prefrontal Cortex: Maintenance vs Manipulation Processes

Cognitive theories of "executive function" vary greatly in the number of distinct cognitive processes they propose to subserve the goal-directed coordination of behavior. Some theories suggest that strong active maintenance of information, and a way of "updating" the information that is maintained, is sufficient to explain performance on executive function (EF) tasks, which typically require careful control over behavior. Other theories propose that a process of "inhibition," distinct from updating and maintenance, must also exist. And then there are those theories that propose yet other components, including shifting, manipulation, monitoring, error- or conflict-detection, etc.

Evidence from factor analyses of executive tasks suggests that there may be at least three executive functions, loosely termed shifting, updating and inhibition. However, individual differences in each of these apparently distinct capacities are inter-correlated, and it has been suggested that differences in active maintenance may account for this shared variance.

There is some evidence that "manipulation" processes may be distinct from maintenance, both from repetitive transcranial magnetic stimulation research as well as developmental work on task-switching. Note that the tasks used in both studies seem similar to the tasks used to tap "updating" in the factor analysis mentioned above. However, there are reasons to be cautious about interpreting the results of both those studies.

Other evidence for the dissociability of maintenance and manipulation processes can be found in a recent article by Crone et al. in PNAS. In this article, Crone et al. had 50 subjects, aged 8 to 25, perform a simple task in which they were asked to remember 3 items over a 6-second delay. During half of the trials, the subjects were asked to repeat the items in the display in a forwards or backwards order. After 6 seconds had elapsed, subjects were asked whether a certain picture had appeared 1st, 2nd or 3rd in the original display of 3 items. This judgment was thought to require only maintenance processes when subjects were rehearsing the items in forward order, but to require manipulation in addition to maintenance when subjects were rehearsing the items in a backward order.

As expected, the results showed that while errors and reaction times on both types of tasks increased with age, the improvement was greater in the more difficult "backwards" condition (the one assumed to require both manipulation and maintenance).

Adults more strongly activated two prefrontal areas (left ventrolateral prefrontal cortex [vlPFC] and bilateral dorsolateral prefrontal cortex[dlPFC]) in the "maintenance + manipulation" backwards task relative to the "maintenance only" forwards task, but the same contrast showed no differences in the younger age groups.

More focused "region-of-interest" analyses revealed that there were no age-differences in the recruitment of vlPFC. In contrast, adolescents and adults showed more dlPFC activation than children during the delay period of the "maintenance + manipulation" trials as compared to "maintenance only" trials. The degree of dlPFC activation predicted performance on the manipulation + maintenance task, whereas degree of vlPFC activation did not.

However tempting, these results are not consistent with a straightforward mapping between maintenance & vlPFC and manipulation & dlPFC: vlPFC was also sensitive to manipulation demands.

This research confirms that the functions subserved by dorsolateral prefrontal cortex are particularly important when cognitive demands are highest, as when information must be simultaneously manipulated and maintained. These results also suggest that dlPFC is one of the last prefrontal areas to show adult-like patterns of activity, as indicated by previous work. Furthermore, it seems that this maps well onto the "updating" tasks identified in previous factor analyses, which were shown to strongly correlate with fluid intelligence.

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