Co-ordination within and between verbal and visuospatial working
memory: network modulation and anterior frontal recruitment
A. Ku ¨bler,
a
K. Murphy,
a
J. Kaufman,
b
E.A. Stein,
b,1
and H. Garavan
a,b,
*
a
Department of Psychology and Institute of Neuroscience, Trinity College Dublin, Dublin 2, Ireland
b
Department of Psychiatry and Behavioral Medicine, Medical College of Wisconsin, Milwaukee, WI 53226, USA
Received 31 March 2003; revised 17 June 2003; accepted 30 June 2003
Abstract
Attention switching between items being stored and manipulated in working memory (WM) is proposed to be an elementary executive
function. Experiment 1 reveals a similar attentional limitation within and between verbal and visuospatial WM and identifies a supramodal
switching process required for switching between WM items. By using functional magnetic resonance imaging, Experiment 2 investigated
brain activation correlates of parametrically varied attention switching within and between these two WM modalities. Attention switching
activation was broadly distributed, was quite similar across the three conditions, and, in almost all areas, increased with increasing switching
demand, indicating that attention switching recruits and modulates the entire WM network. Dorsolateral prefrontal cortex was implicated
in both within- and between-modality attention switching, but no significant activation was found in ventrolateral areas, supporting
dorsal-ventral process models of prefrontal organization. A functional dissociation between anterior frontal and dorsolateral prefrontal
cortex was found with the former being more activated when switching attention between modalities was required. The data challenge the
notion of an anatomically separate attention switching executive function, but suggest that anterior frontal areas are recruited for the
additional demand of coordinating the verbal and visuospatial WM slave systems.
© 2003 Elsevier Inc. All rights reserved.
Introduction
According to current models of working memory, two
separable systems for verbal and visuospatial information
processing are controlled by a central executive, which
allocates attentional resources according to the task require-
ments (Cocchini et al., 2002; Cowan, 1993; Shallice and
Burgess, 1996). Following Baddeley and Hitch (1974), ver-
bal information is processed within the phonological loop
and visuospatial information in the visuospatial sketch pad
(Baddeley and Hitch, 1974). Tasks which engage verbal
working memory have been shown to activate a widespread
network in the brain including dorsolateral prefrontal cortex
(DLPFC), Broca’s area, premotor and supplementary motor
area, anterior cingulate, parietal cortex and cerebellum
(Jonides et al., 1998). For example, Paulesu and colleagues
(Paulesu et al., 1993) localized the phonological store to the
left supramarginal gyrus and the articulatory rehearsal pro-
cess to Broca’s area. As in verbal working memory, tasks
addressing visuospatial working memory activate multiple,
widely distributed regions in parietal, motor, and prefrontal
cortices (Haxby et al., 2000).
While the exact role of the prefrontal cortices in working
memory remains unclear, a number of distinct models have
been proposed. According to one domain-specific model,
the prefrontal cortex is functionally subdivided into a dor-
solateral region for spatial information and a ventrolateral
region for object information (Courtney et al., 1996; Gold-
man-Rakic, 1996). An alternative model argues instead for
domain specificity across hemispheres, wherein a left mid-
frontal area is specialized for object or verbal (non-spatial)
working memory and right inferior and superior frontal
areas for spatial working memory (Smith et al., 1996; Un-
gerleider et al., 1998). Yet a third process-specific model
* Corresponding author: Fax: +353-1-671-2006.
E-mail address: Hugh.Garavan@tcd.ie (H. Garavan).
1
Current address: National Institute on Drug Abuse-IRP, Neuroimag-
ing Research Branch, 5500 Nathan Shock Drive, Baltimore, MD 21224,
USA.
NeuroImage 20 (2003) 1298 –1308 www.elsevier.com/locate/ynimg
1053-8119/$ – see front matter © 2003 Elsevier Inc. All rights reserved.
doi:10.1016/S1053-8119(03)00400-2