Elsevier

Progress in Neurobiology

Volume 116, May 2014, Pages 66-86
Progress in Neurobiology

The cross-functional role of frontoparietal regions in cognition: internal attention as the overarching mechanism

https://doi.org/10.1016/j.pneurobio.2014.02.002Get rights and content

Highlights

  • We compare findings of frontoparietal activation across four cognitive functions.

  • We argue that this activation partly reflects internal attention processes.

  • Task-specific frontoparietal activations are related to internal representations.

  • We develop a neural model of cognitive functions emerging from internal attention.

Abstract

Neuroimaging studies have repeatedly reported findings of activation in frontoparietal regions that largely overlap across various cognitive functions. Part of this frontoparietal activation has been interpreted as reflecting attentional mechanisms that can adaptively be directed towards external stimulation as well as internal representations (internal attention), thereby generating the experience of distinct cognitive functions. Nevertheless, findings of material- and task-specific activation in frontal and parietal regions challenge this internal attention hypothesis and have been used to support more modular hypotheses of cognitive function. The aim of this review is twofold: First, it discusses evidence in support of the concept of internal attention and the so-called dorsal attention network (DAN) as its neural source with respect to three cognitive functions (working memory, episodic retrieval, and mental imagery). While DAN activation in all three functions has been separately linked to internal attention, a comprehensive and integrative review has so far been lacking. Second, the review examines findings of material- and process-specific activation within frontoparietal regions, arguing that these results are well compatible with the internal attention account of frontoparietal activation. A new model of cognition is presented, proposing that supposedly different cognitive concepts actually rely on similar attentional network dynamics to maintain, reactivate and newly create internal representations of stimuli in various modalities. Attentional as well as representational mechanisms are assigned to frontal and parietal regions, positing that some regions are implicated in the allocation of attentional resources to perceptual or internal representations, but others are involved in the representational processes themselves.

Introduction

In cognitive science, concepts like working memory, episodic memory, and mental imagery have generally been investigated in isolation, independent from one another. In neuropsychology, they are assessed with rather different test batteries, and efforts have been made to assign the discrete cognitive functions to separate brain regions (Lezak, 2012). However, findings from brain imaging indicate that the structural and functional make-up of the human brain does not comply with these conceptual differentiations. A major review of brain imaging studies has shown that many cognitive functions appear to share common brain circuits, as they are all associated with the activation of highly similar brain regions when investigated with positron emission tomography or functional magnetic resonance imaging (fMRI; Cabeza and Nyberg, 2000). This finding challenges our understanding of the cognitive concepts under inspection. While the various cognitive functions had up to that point been considered as largely independent processes, the results of the review suggest that especially higher cognitive functions share certain overarching mechanisms and may thus not be as fundamentally different as they are treated on the cognitive-behavioural level.

A network of frontal and parietal brain regions comprising the presumed human homologue of the frontal eye fields (FEF) and the intraparietal sulcus (IPs) extending into the superior parietal lobe (SPL) represents a prime example of such a scenario, as it appears to be involved in mental imagery (e.g., Formisano et al., 2002, Ganis et al., 2004, Ishai et al., 2000, Sack and Schuhmann, 2012, Sack et al., 2008, Sack et al., 2002) working memory (e.g., Collette et al., 2007, Curtis, 2006, Gordon et al., 2012, Linden et al., 2012, Majerus et al., 2010; Owen et al., 2005, Passaro et al., 2013, Pessoa et al., 2002, Postle et al., 2004, Rottschy et al., 2012), and episodic memory retrieval (e.g., Burianová et al., 2012, Ciaramelli et al., 2010, Kim, 2010, Kragel and Polyn, 2014, Kwok et al., 2012, Ranganath et al., 2005; see Fig. 1 for overlapping patterns of activation across tasks).

This suggests that this network supports one broader mechanism that is needed for the execution of all these functions, rather than several task-specific processes. The challenge is to identify the mechanism that underlies these functions in their essence and to understand how this cognitive-behavioural essence is represented in the brain. A likely candidate for this overarching mechanism is that of attention, more specifically top-down attentional orienting or attentional control. For one thing, in neuroscience, the activation of FEF and IPs has been strongly implicated in specific processes of attentional orienting (Corbetta and Shulman, 2002) and is quite consensually labelled the dorsal attention network (DAN; see Corbetta et al., 2008, Power et al., 2011). Furthermore, from a purely cognitive perspective, attention can be considered one of the most basic mechanisms, likely to be involved in the successful execution of almost all cognitive tasks. It thus seems plausible to assume that the recurring activation of the FEF and IPS (as a network) across cognitive tasks is related to the attentional demands these tasks entail.

The finding of DAN activation across tasks involving the internal maintenance or representation of task material has nurtured a set of neurocognitive models that focus on attentional orienting as a central mechanism in the field of working memory (internal attention; e.g., Lepsien and Nobre, 2007, Nobre et al., 2004), episodic retrieval (attention to memory; e.g. Cabeza et al., 2008, Ciaramelli et al., 2008), and mental imagery (top-down control; e.g., Kosslyn, 2005, Sack and Schuhmann, 2012, Zimmer, 2008).

The common quintessence of these accounts is that the respective cognitive functions are all assumed to involve the orienting of attentional resources towards internal representations of task-relevant material. On the neural level, this task-relevant material is assumed to be represented in the brain regions initially involved in the sensory processing of that same material, and the attentional mechanism originating in the DAN is conceptualised as a top-down modulation or biasing of these sensory processing regions to maintain or reactivate the neural activation that encodes the material. Rather than proposing a multitude of functionally specific modules within the brain, these models thus suggest a more parsimonious view of brain function, where the same attentional mechanisms can be adaptively applied to a multitude of external and internal processes. In line with this, the past decade of fMRI studies has furthermore brought forward accumulating evidence that the execution of working memory, episodic retrieval, and mental imagery tasks is associated with activation in regions involved in sensory processing of the material used during the tasks (e.g., Majerus et al., 2010, Van de Ven and Sack, 2013, Borst and Kosslyn, 2008, for working memory, episodic retrieval, and working memory, respectively) and that this activation is sustained in the absence of sensory stimulation and likely modulated by the DAN (e.g., Lee and D’Esposito, 2012). Over and above, there is evidence that the same visuospatial attentional mechanisms that are applied to external events can also be directed to internal representations of visual material (e.g., Griffin and Nobre, 2003).

In spite of the above summarised evidence in support of attention-based conceptualisations of cognitive functions, these concepts have repeatedly been challenged by proponents of the more traditional (and originally cognitive) models of the three cognitive functions that adhere to process-specific modules and material-specific stores or buffers, particularly in the field of episodic memory and working memory research (Atkinson and Shiffrin, 1968, Baddeley, 2000, Baddeley and Hitch, 1974; see also Jonides et al., 2008). In trying to transfer these models to neuroscience, several researchers have set forth to link the modules (or “boxes”) and processes described in their models to specific circumscribed brain regions. Indeed, neuroimaging has provided evidence for process- and material-specific activation in frontal and parietal association cortex during working memory (Rottschy et al., 2012, Smith and Jonides, 1998, Smith et al., 1996), episodic retrieval (e.g., Buckner and Wheeler, 2001, Guerin and Miller, 2011, Vilberg and Rugg, 2008), and mental imagery (Daselaar et al., 2010, Kosslyn and Thompson, 2003, Zvyagintsev et al., 2013) and these regions have consequently been put forth as the possible neural substrates of the material- and process-specific modules described in the models of the respective cognitive function (e.g., Baddeley, 2003, Vilberg and Rugg, 2008).

While process- and material-specific activation in frontal and parietal association cortex is therefore often regarded as counter-evidence of attentional models of working memory, episodic memory, and mental imagery, we argue that such activation is fully compatible with the internal attention account, if one assumes that the frontal and parietal regions displaying material- or process-specific activation are actually the sites modulated by the attentional processes, i.e., reflecting the locus of the at that time maintained or reactivated internal representation. It is the aim of the current paper to discuss the evidence in favour of a possible role of frontoparietal regions in internal attention processes using the examples of three related cognitive functions; working memory, episodic retrieval, and mental imagery. We also discuss findings of process- and material-specific activation in these regions and provide a framework that allows for the integration of these findings.

Starting with a discussion of the task-general involvement of frontoparietal regions in cognition, we first outline the proposed function of the DAN in attentional orienting and then show how the neural mechanisms of attentional orienting to the external world can be applied to internal processes as well (Section 2.1). We then elucidate how three cognitive processes—working memory, episodic memory retrieval, and mental imagery—can be conceptualised as deriving from attentional processes directed at internal representational processes and will also outline why the DAN likely plays a central role in the control and allocation of these attentional processes across cognitive functions (Section 2.2). We then go on to explain why findings of process- or material-specific activation within frontal and parietal regions inside and outside the DAN are not incompatible with the proposed attention-based models of cognitive function, and how they may instead represent particular attentional or representational processes (Section 3).

Section snippets

External attention

Based on their review of studies investigating attentional orienting in non-human primates and of neuroimaging data of the same processes in humans, Corbetta and Shulman (2002) proposed a model of visuospatial attention that located the neural basis of attentional orienting and reorienting within a set of frontoparietal regions comprising the FEF, parts of middle frontal gyrus (MFG) and inferior frontal gyrus (IFG), the IPs extending into SPL, part of the inferior parietal lobe (IPL; mainly

Task-specific activation

While the internal attention account can nicely explain the overlapping DAN activation in the investigated cognitive functions, it is challenged by findings of material- or process-specific activation within the DAN and in proximal frontoparietal brain regions. These findings have corroborated other theories about the role of frontoparietal regions that are often task-specific in nature and are competing with the attention-related account. In the following, we will argue how these findings are

Overall summary and relation to previous concepts

In this review we support the view that cognitive functions like working memory, episodic memory retrieval, and mental imagery do not rely on their own function-specific neural systems but do all result from the interaction of multiple overlapping brain regions. More specifically, we propose that all three functions emerge when attentional mechanisms implemented in the DAN direct attention to brain areas that have evolved to process the material that has to be represented in the task at hand.

Conflict of interest

The authors declare no conflict of interest.

Acknowledgement

The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement no. [263472]; granted to A.T.S.).

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