The studies described earlier suggested that the processes supported by rostral PFC are involved in PM and therefore multitasking. This is useful in understanding how the brain supports these ‘functions’ (i.e. behaviours understood in context of (i) a goal and (ii) a task analysis; see Burgess et al. 2006a
for explanation). However, area 10 has been implicated as important in supporting many other functions, such as recollection or reflecting on mental states (see Grady 1999
; Ramnani & Owen 2004
; Gilbert et al. 2006a
for review). It therefore seemed plausible that different subsections of area 10 support quite different functions. However, an account of this type raises two problems. The first is the possibility of infinite explanatory regress. Most functions will have sub-functions (or sub-operations) and the localization of each is likely at some level to be different. Moreover, one would be unlikely to discover processing common to many functions with this approach. The second problem is that starting with an assumption of strong modular functional specialization may leave the discovery of the relevant functions essentially to chance. Accordingly, in order to provoke new hypotheses, we proceeded on the basis of the simplifying assumption that BA 10 may support some critical processing component (or ‘construct’) which is shared by all the implicated functions (for definition of the terms function and construct in this context, see Burgess et al. 2006a
The challenge was to find a function that fitted the myriad of observations from functional imaging and also those from the human lesion data. This was not straightforward, in particular because the findings from the two methods seemed to present a conundrum. This was that, based on the functional imaging findings of BA 10 activation in a wide range of tasks, an obvious suggestion might be that BA 10 supports some cognitive processing that is important to the performance of all of them. But if this were the case, then one would expect to see performance deficits across a correspondingly wide variety of tasks when this region is damaged in humans. However, this is not the case. As we have seen, neurological patients with rostral PFC lesions need not show impairments on tests of intelligence, clinical (retrospective) memory tests, language, perception and even tests of executive function such as the Wisconsin Card Sorting Test, FAS fluency, etc.
An appropriate account had to accommodate this apparent conundrum and also to be compatible with the other sets of constraints for theorizing presented by these different methods. Burgess et al. (2005)
list the constraints we took as a starting position. There were seven constraints from human lesion studies and 17 from the functional imaging literature. Examples of the former were: ‘rostral PFC lesions disproportionately impair performance in ‘ill-structured’ situations, in other words where the optimal way of behaving is not precisely signalled by the situation’; and ‘rostral PFC lesions need not markedly impair performance on standard tests of intelligence, especially those that measure ‘crystallized’ intelligence, or those involving the use of over-learned procedures (e.g. arithmetic)’. Examples of the constraints for theorizing presented by the functional imaging literature were, for example, ‘rostral PFC activation is not sensitive to the precise nature of stimuli, the nature of the intended action (in PM tasks) nor the precise response method, but is consistently implicated in tasks where one has to ‘bear something in mind’ while doing something else’.
The account that emerged as a potential solution was termed the ‘gateway hypothesis’ (Burgess et al. 2003
). This theory of the role of BA 10 in human cognition rests upon a distinction between stimulus-oriented (SO) and stimulus-independent (SI) attending (McGuire et al. 1996
). SO attending refers to the attending behaviour that is required to concentrate on current sensory input. (Here, we make a distinction between ‘attention’ as a construct (i.e. a hypothetical processing resource that may operate across a range of operations or functions), and attending behaviour as a function or operation (function, directly observable behaviour; operation, mental experience) that may be indirectly inferred from observation; e.g. if presented with the sum 2+4 and a person responds ‘6’, one might infer that they have performed a calculation operation; see Burgess et al. 2006a
Examples of SO attending range from performance of vigilance tasks, to reading, watching the television, listening to a conversation and so forth. By contrast, SI attending is the attending behaviour required to effect either self-generated or self-maintained thought. Self-generated thought is cognition that goes beyond the overlearned associations or semantic memories provoked by currently available stimuli. In this respect, the concept shares similarities with that of N-order (i.e. second order, third order, etc.) representations used in experimental and developmental psychology and artificial intelligence. By contrast, self-maintained thought is where one deliberately maintains a representation in the absence of the stimuli that provoked it. It is the absence of the stimulus that provoked the representation that defines this operation as belonging to the class of ‘SI’ cognition. Examples of SI cognition therefore range from task-irrelevant thoughts such as mind-wandering or daydreaming, to goal-directed cognition such as that involved in making up a novel story, or maintaining a representation over a delay period, and so forth.
We assume that many mental experiences which occur over all but the briefest of durations will consist of combinations of SO and SI attending. Accordingly, for empirical purposes, data relating to an SO or SI distinction might be thought of as existing along a continuum of relative proportions of variance. However, at the extremes at least, the distinction may be robust enough for empirical purposes. For instance, we describe four characteristics with which one can imbue a task that would increase the relative demand for SO attending, compared with a task that did not have these characteristics (Burgess et al. submitted a
- Requires vigilance (e.g. attending in absence of stimulus or attentional capture).
- Requires stimulus processing, i.e. awareness of stimulus characteristics (e.g. as required for conditional responding of the form ‘if characteristic X, then respond Y’).
- The information required to respond appropriately is currently available. For instance, the task that presents subjects with maths problems of the form ‘4+2=’ will be a purer measure of SO attending than one that requires comparing the sum of the currently presented numbers with the sum of two previously (but not currently) seen.
- The operations involved prior to responding are automatic, well learnt or involve retrieval from semantic memory only (i.e. they are not novel).
Similarly, one might describe characteristics with which one might imbue a task which would increase the relative demand for SI attending, thus:
- The task encourages mind-wandering, for example, by being easy, monotonous, non-novel and repetitive.
- All the information required to respond appropriately is not currently being presented, and:
- The information that is required in order to respond appropriately is not well learnt or from semantic memory, but comes from a previously witnessed episode (e.g. as in a delay task).
- The task requires the use of self-generated representations (e.g. novel problem solving, imagination).
- The task requires working with representations that were self-generated on a previous occasion and have not been rehearsed in the meantime.
It is important to note that these are not the only characteristics one might outline. An everyday example to demonstrate the contrast between SO and SI modes of attending might be where one is trying to concentrate on a rather dull lecture (SO attending) versus imagining what one might do that evening after the lecture (SI attending). The gateway hypothesis proposes that rostral PFC in part supports a system which operates when one is required to maintain either mode of attending to an unusual degree or switch between them. More specifically, it proposes that medial rostral PFC plays a role in supporting SO attending, and lateral rostral PFC facilitates switching to, maintaining and voluntarily switching away from, SI cognition (). In this way, the cognitive system supported by rostral PFC was characterized as a ‘gateway’ between mental life and the external world. (For related accounts from neuroimaging, see McGuire et al. 1996
; Christoff & Gabrieli 2000
; Christoff et al. 2001
; Pollmann 2001
; Mason et al. 2007
.) Within the information processing framework of Shallice & Burgess (1996)
, it is assumed that this attentional system lies between the contention scheduling (routine schema selection) and the other supervisory system modules (controlled processing), effecting bias between them (see also Shallice & Burgess 1991b
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 (more ...)
This potential account, if true, might solve the apparent conflict between the imaging and lesion evidence since (i) the attentional ‘gate’ would operate in a wide variety of tasks, but not be critical to the performance of tasks that involve routine, informationally encapsulated processing resources or where attending is strongly driven by the environment, (ii) the difficulties that patients with rostral PFC damage experience (e.g. with multitasking and PM) are those that are particularly likely to require the operation of the attentional gate. This is because both multitasking tasks of the type investigated here (i.e. where one task is carried out while bearing in mind that one has to voluntarily switch to another soon) and also typical PM paradigms, both require active intention maintenance (SI cognition) while also engaging with external stimuli (SO attending) in performance of the ongoing task, or current subtask.