Overlapping functional anatomy for working memory and visual search

Abstract

Recent behavioural findings using dual-task paradigms demonstrate the importance of both spatial and non-spatial working memory processes in inefficient visual search (Anderson et al. in Exp Psychol 55:301-312, 2008). Here, using functional magnetic resonance imaging (fMRI), we sought to determine whether brain areas recruited during visual search are also involved in working memory. Using visually matched spatial and non-spatial working memory tasks, we confirmed previous behavioural findings that show significant dual-task interference effects occur when inefficient visual search is performed concurrently with either working memory task. Furthermore, we find considerable overlap in the cortical network activated by inefficient search and both working memory tasks. Our findings suggest that the interference effects observed behaviourally may have arisen from competition for cortical processes subserved by these overlapping regions. Drawing on previous findings (Anderson et al. in Exp Brain Res 180:289-302, 2007), we propose that the most likely anatomical locus for these interference effects is the inferior and middle frontal cortex of the right hemisphere. These areas are associated with attentional selection from memory as well as manipulation of information in memory, and we propose that the visual search and working memory tasks used here compete for common processing resources underlying these mechanisms.

Fig. 1

Search stimuli. Visual search stimuli comprised a uniform grey background with an array of randomly rotated white letter L distractors equally spaced in a concentric ring, around a central white fixation cross. On target present trials one of the distractors was replaced by a randomly rotated letter T. Participants were required to report the presence or absence of the rotated letter T as fast and as accurately as possible. Two set sizes were used, n = 4 (T4) and n = 10 (T10)

Fig. 2

Visually matched spatial working memory and verbal working memory tasks. Example trial sequences for experiment 1 (a) SWM only and (b) VWM only. For the SWM only task participants were instructed to remember the locations of the letters (and the temporal order in which they were presented), but to ignore the identity of the letters. For the VWM only task participants were instructed to remember the identity of the letters, but to ignore the locations in which they appeared. The sequence of locations/letters had to be retained across a 2,500 ms interval after which a probe screen appeared. Participants were instructed to make a button response ‘yes’ or ‘no’ to indicate whether the central number corresponded to the temporal position in which that location (SWM)/letter (VWM) had been presented (see “Methods”). Previous data confirms that these tasks are matched for task difficulty (Anderson et al. 2008)

Fig. 3

Results Experiment 1—the effects of dual-task performance on search times. RTs for inefficient search performed in isolation have been subtracted from search RTs during the dual-task conditions, for target present (filled triangle) and target absent search (filled square). On average, an additional 11 ms per item was required to perform target present search concurrently with the SWM task and 26 ms per item for target absent search, compared to search performed in isolation. Similarly an extra 11 ms per item was required for target present search performed concurrently with the VWM task and 28 ms per item for target absent search. Error bars indicate standard error of the mean

Fig. 4

Four blocked experimental conditions used in the fMRI paradigm. Example trials from the four experimental conditions: (a) SWM only, (b) VWM only, (c) SWM & search, (d) VWM & search. A cue screen appeared at the beginning of each block, indicating which task to perform for the following four trials. All conditions were matched for visual and motor responses. For the working memory only trials (a, b) a target absent visual search array was presented during the retention interval (instead of just a fixation cross used in experiment 1). The colour of the fixation cross changed from white to black to remind participants NOT to search, and subjects were asked to always report target absence. For the dual-task trials (c, d), subjects were required to perform the visual search task, whilst simultaneously rehearsing information required for the working memory task

Fig. 5

Common areas activated by inefficient search and both working memory tasks. a 3D rendering of a standardised T1 brain template with superimposed loci of brain activity showing areas in the brain which are commonly activated by the spatial working memory, verbal working memory and inefficient visual search. b Axial slices of a standardised brain template showing overlapping regions of activity for inefficient visual search (blue), spatial working memory (red) and verbal working memory (green). A threshold of p < 0.005 has been used for illustrative purposes, but all clusters were significant to p < 0.001 (except L IFG). (c) Coordinates of activation maxima for regions of overlap and approximate Brodmann’s Areas (BA)

Fig. 6

Region of interest analyses in R MFG and R IFG. Sagittal, coronal and axial views of the right IFG ROI (a) and right MFG ROI (b). These regions were defined apriori using the results of our previous fMRI study on inefficient search (Anderson et al. 2007). The right IFG region was defined by a cluster of activity centered around the MNI coordinates [44/20/-6] (see “Methods”). The right MFG region was defined by a sphere with a 15 mm radius centered on the MNI coordinates [48/12/26]. The bar graphs represent parameter estimates for spatial (blue) and verbal (green) working memory, for single and dual-task conditions, within these two regions. Error bars indicate the SE of the mean for the group