Frontal lobes and human memory 855 mply to heneve T a prespe of information viewed as propo rtional to theworking memory load'the istent with neuroimaging studies of spatial attention total demand placed on the maintenance and/or manipulation of the pro nd colle Coull and 1998)A tentativ hypothesis is tha visuospatial information is stored as abstract or object visua representations in the occipital cortex and inferor tempora linearly increasing functi aps com well as nted by as between these areas and the righ rea On the ad parietal cortex. associations that may be refreshed by a process above.the VLFC.posterior parietal and motor activations sequenti network of areas involved in th arsal of the mo In summary,imaging studies have produced good evidence findings implicate the additional bilateral activation of DLFC for material-specific in manipulation (e.g.updating of the particular letters being udy Smit y to sus studies ver ther ted bilat DLFC/AFC activations in both a verbal is little imaging evide e for ventral-dorsal object -spatia no task in human vation i obiect inf left-lat tudy owen Sn6 nd c and that for the maintenance of spatial information.Th back tasks (Owen).Although differences betv een gion mos consistently the spatial and object memory-relate we as th p infor for the object task the coordinates of the DLFC is also sometime peaks of the bilateral DLFC/AFC activations for the two et al.,1996a:Belger et al..1998) SKS within a pr ght al int Manipulation in working memory ses in vlEC but that maninulation p he Manipulation of the contents of WM involves n array of nmon to visual- tial and visual-obiect WM.These two processe that may b unde the headin que the M sed and a huse nge of diffe onmateral-specine en tasks have been examined.Without attempting a precis FC lateralization of different executive processes. we Cohen and colleagues attempted to dissociate maintenanc on broad have be 'dual'and planning tasks.We emphasize that these term (Cohen et al 1997)Brain regions involved in transien are descriptive of the type of task employed and are not such ceiving stimu meant to imply different sets of executive processe isual and m N-back tasks such as maintenance,were predicted to show an uask that combine and manipulation isthe These regions inclu ask (Fig tas requires the right DLF Region whe ever the current stimulus matches the stimulusp mantain.were predicted to show an inter on between load tions back in the quence.For n 0.this task requires t an I time (i.e.greater transient effects at higher loads).The maintenance of the last n stimuli (in order)and updating of only lateral prefront region to shov this pattem was Frontal lobes and human memory 855 eye fields, the pulvinar nucleus or superior colliculus are not these stimuli each time a new stimulus occurs (for n
0 the typically observed in neuroimaging studies of visuospatial task is simply to respond whenever a prespecified target WM. Another possibility, that rehearsal of visuospatial occurs, thus no updating is required). The value of n is often information involves an internal attentional mechanism, is viewed as proportional to the ‘working memory load’—the consistent with neuroimaging studies of spatial attention, total demand placed on the maintenance and/or manipulation which activates similar areas of the right superior parietal processes. cortex independently of eye movement (Corbetta et al., 1993; Braver and colleagues varied the verbal WM load by Coull and Nobre, 1998). A tentative hypothesis is that increasing n from 0 to 3 in a letter version of the n-back visuospatial information is stored as abstract or object visual task (Braver et al., 1997). Areas in which activity was a representations in the occipital cortex and inferior temporal linearly increasing function of load included DLFC, VLFC cortex, respectively (perhaps corresponding to visual caches). and the parietal cortex, bilaterally in each case, as well as a The (egocentric) spatial organization of the stimuli may be number of left motor, premotor and supplementary motor represented by associations between these areas and the right areas. On the basis of the maintenance studies reviewed parietal cortex, associations that may be refreshed by a process above, the VLFC, posterior parietal and motor activations of sequential, selective attention (perhaps corresponding to are likely to reflect the network of areas involved in the an inner scribe) that engages the right superior parietal cortex, maintenance of verbal information (e.g. the storage and right premotor cortex and right FC. rehearsal of the most recent n letters). If this is so, then these In summary, imaging studies have produced good evidence findings implicate the additional bilateral activation of DLFC for material-specific stores in posterior brain regions and in manipulation (e.g. updating of the particular letters being some evidence for a left–right lateralization of FC regions for maintained). the rehearsal of verbal and spatial information, respectively. In another study, Smith and colleagues (Smith et al., 1996) Contrary to suggestions from primate studies, however, there reported bilateral DLFC/AFC activations in both a verbal is little imaging evidence for ventral–dorsal object–spatial and spatial 3-back task, though there is a tendency for greater distinction in non-verbal maintenance tasks in humans. left DLFC activation in the former and greater right DLFC Rather, FC activation associated with the maintenance of activation in the latter (Smith and Jonides, 1997). In a similar object information appears to be more left-lateralized relative study, Owen and colleagues compared spatial and object 2- to that for the maintenance of spatial information. The back tasks (Owen et al., 1998). Although differences between FC region most consistently associated with the simple the spatial and object memory-related activations were maintenance of verbal material is the left VLFC. The VLFC observed in posterior regions, such as the posterior parietal is often associated with the maintenance of spatial and object cortex for the spatial task and the middle and anterior information (on the right for spatial information), though temporal cortex for the object task, the coordinates of the DLFC is also sometimes activated in these cases (e.g. Baker peaks of the bilateral DLFC/AFC activations for the two et al., 1996a; Belger et al., 1998). tasks were within 2 mm of each other. These data suggest that manipulation processes in DLFC are left–right lateralized for verbal versus spatial information, as for maintenance Manipulation in working memory processes in VLFC, but that manipulation processes may be Manipulation of the contents of WM involves an array of common to visual–spatial and visual–object WM. These two processes that may be loosely grouped under the heading studies again question the specific dorsal–ventral spatial– of executive processes. Many different types of executive object FC dissociation suggested by Goldman-Rakic, processes have been proposed and a huge range of different though support a material-specific left–right verbal–spatial tasks have been examined. Without attempting a precise FC lateralization. definition of different executive processes, we concentrate Cohen and colleagues attempted to dissociate maintenance below on broad categories of manipulation task that have been and manipulation in an n-back task by using event-related used in neuroimaging: ‘n-back’, ‘reordering’, ‘generation’, fMRI to measure activity at four intervals after each trial ‘dual’ and ‘planning’ tasks. We emphasize that these terms (Cohen et al., 1997). Brain regions involved in transient are descriptive of the type of task employed and are not processes, such as perceiving stimuli and producing meant to imply different sets of executive processes. responses, were predicted to show an effect of time but no effect of load (n). As expected, these regions included the visual and motor cortices. Regions involved in sustained N-back tasks processes, such as maintenance, were predicted to show an A task that combines maintenance and manipulation is the effect of load but not time. These regions included bilateral N-back task (Fig. 2D). This task requires the monitoring of VLFC and right DLFC. Regions associated with transient a continuous sequence of stimuli; a positive reponse occurs manipulation processes, such as updating the n items to whenever the current stimulus matches the stimulus n posi- maintain, were predicted to show an interaction between load tions back in the sequence. For n 0, this task requires both and time (i.e. greater transient effects at higher loads). The maintenance of the last n stimuli (in order) and updating of only lateral prefrontal region to show this pattern was left