Function and localization within rostral prefrontal cortex (area 10)

Abstract

We propose that rostral prefrontal cortex (PFC; approximating area 10) supports a cognitive system that facilitates either stimulus-oriented (SO) or stimulus-independent (SI) attending. SO attending is the behaviour required to concentrate on current sensory input, whereas SI attending is the mental processing that accompanies self-generated or self-maintained thought. Regions of medial area 10 support processes related to the former, whilst areas of lateral area 10 support processes that enable the latter. Three lines of evidence for this 'gateway hypothesis' are presented. First, we demonstrate the predicted patterns of activation in area 10 during the performance of new tests designed to stress the hypothetical function. Second, we demonstrate area 10 activations during the performance of established functions (prospective memory, context memory), which should hypothetically involve the proposed attentional system. Third, we examine predictions about behaviour-activation patterns within rostral PFC that follow from the hypothesis. We show with meta-analysis of neuroimaging investigations that these predictions are supported across a wide variety of tasks, thus establishing a general principle for functional imaging studies of this large brain region. We then show that while the gateway hypothesis accommodates a large range of findings relating to the functional organization of area 10 along a medial-lateral dimension, there are further principles relating to other dimensions and functions. In particular, there is a functional dissociation between the anterior medial area 10, which supports processes required for SO attending, and the caudal medial area 10, which supports processes relating to mentalizing.

Figure 1

(a) Materials for the Modified Six Element Test (Burgess et al. 1996). Participants are given 10 minutes to complete at least some of each of the three subtasks, each divided into two parts (i.e. verbal dictation A and B, picture naming A and B, arithmetic A and B), but are not permitted to perform two subtasks of the same type straight after each other (e.g. arithmetic A then arithmetic B). (b) Lesion overlap figure from Burgess et al. (submitted b) for a group of right rostral PFC-damaged participants who made fewer task switches than other patients or healthy controls on a new version of the Six Element Test (right rostrals: mean voluntary task switches 3.0 (s.d. 2.1), other patients mean 6.3 (s.d. 4.0), p<0.005).

Figure 2

Stylized representation of the ‘gateway hypothesis’ of rostral prefrontal function. Rostral PFC regions are hypothesized to support a system that biases the flow of information between basic systems and central representations (i.e. equivalent to the adjustment of the position of the ‘gates’). The gates are shown in the neutral position (equal to bias freely determined by context). If both gates are at position A, SI cognition is favoured. If both gates are at position B, full engagement with (external) stimuli is effected. Other combinations have further experiential correlates, especially when one considers dynamic, moment-by-moment switching. The operation of processes supported by lateral rostral PFC would correspond to the effecting of both gates to position A, with the operation of anterior medial rostral PFC regions effecting movement towards position B. However, this cartoon should not be taken too literally. The main purpose of the diagram is to emphasize how even a very simple switch system could effect a range of mental activity. Many other types of analogy could be used.

Figure 3

(a) Results from Burgess et al. (submitted a). Tasks requiring SO attending only are contrasted with tasks requiring SO attending plus SI attending (see text for details of the tasks). There is increased BOLD signal bilaterally in lateral area 10 in conditions requiring SI attending. Rostral medial area 10 shows the opposite pattern. The regions rendered on the brain (left) are colour coordinated to the graph (right). Coordinates are MNI. Bars are s.e.m. (b) Results from Gilbert et al. (2006a). Regions of activation revealed in the comparison of SO against SI conditions are shown in yellow. Regions where the BOLD signal correlated with reaction time in a separate simple-reaction time baseline condition are shown in red. This shows that BOLD signal in medial rostral PFC was greater on trials with relatively fast reaction times, ruling out an account of the role of this region in terms of task-unrelated thought during low-demand conditions (since this would be expected to compromise reaction time). (RT, reaction time.)

Figure 4

(a) Smoothed RT data from a meta-analysis of 104 functional neuroimaging studies reporting activation peaks in rostral PFC (Gilbert et al. 2006b). On average, contrasts producing activation peaks in regions coloured blue involved faster RTs in the experimental task than the control task against which it was compared. By contrast, those contrasts where the RTs in the experimental condition were slower than in the control condition tended to produce activation peaks in the regions marked in red. This pattern occurred regardless of the type of paradigm under use (e.g. episodic memory, mentalizing, etc.). (b) Results of a second meta-analysis of these 104 studies, which investigated the association between different types of task and the location of activation peaks within rostral PFC (Gilbert et al. 2006c). Note that the studies involving multiple-task coordination tended to yield activation peaks rostral to those involving mentalizing. (c) Results of an fMRI study that crossed the factors of attentional focus (SO versus SI) with mentalizing (mentalizing versus non-mentalizing judgments; Gilbert et al. submitted). The regions of activation in rostral PFC produced by the SO versus SI contrast were rostral to those produced by the mentalizing versus non-mentalizing contrast. In both (b) and (c), the results are plotted on an axial slice (z=24) of the participants' mean normalized structural scan.