Similar and dissociable mechanisms for attention to internal versus external information

Abstract

We compared two attentional executive processes: updating, which involved attending to a perceptually present stimulus, and refreshing, which involved attending to a mentally active representation of a stimulus no longer perceptually present. In separate blocks, participants either replaced a word being held in working memory with a different word (update), or they thought back to a just previously seen word that was no longer perceptually present (refresh). Bilateral areas of frontal cortex, supplementary motor area, and parietal cortex were similarly active for both updating and refreshing, suggesting that a common network of areas is recruited to bring information to the current focus of attention. In a direct comparison of update and refresh, regions more active for update than refresh included regions primarily in right frontal cortex, as well as bilateral posterior visual processing regions. Regions more active for refresh than update included regions primarily in left dorsolateral frontal and left temporal cortex and bilateral inferior frontal cortex. These findings help account for the similarity in areas activated across different cognitive tasks and may help specify the particular executive processes engaged in more complex tasks.

Introduction

A common fronto-parietal network of areas (lateral prefrontal cortex, parietal cortex and supplementary motor area) is active in many cognitive tasks (Cabeza and Nyberg, 2000, Duncan and Owen, 2000) including working memory (WM), visual attention (Kelley et al., 2007, Serences et al., 2005, Serences and Yantis, 2007, Marois et al., 2004), and encoding (Blumenfeld and Ranganath, 2007) and retrieval from long term memory (Cabeza et al., 2008). This similarity of activity is consistent with the idea that common component processes are recruited for diverse cognitive tasks (Duncan and Owen, 2000, Cabeza and Nyberg, 2000, Johnson and Hirst, 1993; see also Awh and Jonides, 2001, Awh et al., 2006). Characterizing these components more specifically is a major challenge for cognitive science.

Two component executive processes that might, in part, account for this common activation across experiments are updating (Roth et al., 2006) and refreshing (Johnson et al., 2005). Updating, the replacement of an item actively being maintained in working memory with a different item, produces activity in a network including left inferior frontal junction (IFJ, the junction of inferior frontal sulcus and inferior precentral sulcus), dorsolateral prefrontal cortex (DLPFC), supplementary motor area (SMA), and bilateral parietal cortex including intraparietal sulcus (IPS). This network becomes active during updating of different types of visual stimuli (Roth et al., 2006), updating from a sensory stimulus or an item from long term memory (Roth and Courtney, 2007), and when the rule operating on a stimulus is updated (Montojo and Courtney, 2008). Refreshing is the process of attending to information that is not perceptually present but is momentarily active from either recent perception or thought (e.g., thinking back to a just-seen stimulus no longer on the screen; Raye et al., 2002; Johnson et al., 2005). Refreshing produces activity in a network including DLPFC, anterior cingulate cortex (ACC), supramarginal gyrus (SMG), IPS, and middle temporal gyrus, for a variety of types of stimuli (Johnson et al., 2005, Raye et al., 2002, Raye et al., 2007).

Similarities in activation for updating and refreshing across experiments have been noted before (Courtney et al., 2007), but this is the first experiment to directly compare them. One possibility is that updating and refreshing are the same process investigated in the context of different experimental paradigms and under different names. If so, we would expect refreshing and updating to produce the same patterns of activation in the same participants in procedures using the same materials. On the other hand, updating has been proposed as a specific mechanism for changing the contents of what is being actively maintained in working memory by prioritizing new information that is concurrently perceived or retrieved. Refreshing has been proposed as a general mechanism for briefly bringing information that is currently active but not perceptually present to the foreground of attention. Update and refresh may involve different areas of cortex. For example, updating should show relatively greater activity in posterior visual processing regions as a new target is perceptually attended, and refreshing should show relatively greater activity in frontal regions (e.g., left DLPFC) associated with modulating representations of no longer present perceptual stimuli (M.R. Johnson et al., 2007).

Assuming that there is a distinction between the cognitive operations and neural activity involved in perceptual vs. reflective attention (e.g., Dobbins and Han, 2006, Gilbert et al., 2005, Johnson et al., 2005, Johnson and Johnson, in press), directly comparing the neural correlates of updating working memory from a perceptually present stimulus with refreshing an active representation of a stimulus that is no longer perceptually present should help clarify similarities and differences in neural activity observed in more complex cognitive tasks that recruit these processes.