Neuroimaging studies of working memory:

We performed meta-analyses on 60 neuroimaging (PET and fMRI) studies of working memory (WM), considering three types of storage material (spatial, verbal, and object), three types of executive function (continuous updating of WM, memory for temporal order, and manipulation of information in WM), and interactions between material and executive function. Analyses of material type showed the expected dorsal-ventral dissociation between spatial and nonspatial storage in the posterior cortex, but not in the frontal cortex. Some support was found for left frontal dominance in verbal WM, but only for tasks with low executive demand. Executive demand increased right lateralization in the frontal cortex for spatial WM. Tasks requiring executive processing generally produce more dorsal frontal activations than do storage-only tasks, but not all executive processes show this pattern. Brodmann’s areas (BAs) 6, 8, and 9, in the superior frontal cortex, respond most when WM must be continuously updated and when memory for temporal order must be maintained. Right BAs 10 and 47, in the ventral frontal cortex, respond more frequently with demand for manipulation (including dual-task requirements or mental operations). BA 7, in the posterior parietal cortex, is involved in all types of executive function. Finally, we consider a potential fourth executive function: selective attention to features of a stimulus to be stored in WM, which leads to increased probability of activating the medial prefrontal cortex (BA 32) in storage tasks.     

The effects of prefrontal lesions on working memory performance and theory

The effects of experimental lesions of the monkey prefrontal cortex have played a predominant role in current conceptualizations of the functional organization of the lateral prefrontal cortex, especially with regard to working memory. The loss or sparing of certain performance abilities has been shown to be attributable to differences in the specific requirements of behavioral testing (e.g., spatial vs. nonspatial memoranda) along with differences in the specific locations of applied ablations (e.g., dorsal vs. ventral prefrontal cortex). Such findings, which have accumulated now for over a century, have led to widespread acceptance that the dorsolateral and ventrolateral aspects of the prefrontal cortex may perform different, specialized roles in higher order cognition. Nonetheless, it remains unclear and controversial how the lateral prefrontal cortex is functionally organized. Two main views propose different types of functional specialization of the dorsal and ventral prefrontal cortex. The first contends that the lateral prefrontal cortex is segregated according to the processing of spatial and nonspatial domains of information. The second contends that domain specialization is not the key to the organization of the prefrontal cortex, but that instead, the dorsal and ventral prefrontal cortices perform qualitatively different operations. This report critically reviews all relevant monkey lesion studies that have served as the foundation for current theories regarding the functional organization of the prefrontal cortex. Our goals are to evaluate how well the existing lesion data support each theory and to enumerate caveats that must be considered when interpreting the relevant literature.     

Defining the cortical visual systems: "what", "where", and "how"

The visual system historically has been defined as consisting of at least two broad subsystems subserving object and spatial vision. These visual processing streams have been organized both structurally as two distinct pathways in the brain, and functionally for the types of tasks that they mediate. The classic definition by Ungerleider and Mishkin labeled a ventral "what" stream to process object information and a dorsal "where" stream to process spatial information. More recently, Goodale and Milner redefined the two visual systems with a focus on the different ways in which visual information is transformed for different goals. They relabeled the dorsal stream as a "how" system for transforming visual information using an egocentric frame of reference in preparation for direct action. This paper reviews recent research from psychophysics, neurophysiology, neuropsychology and neuroimaging to define the roles of the ventral and dorsal visual processing streams. We discuss a possible solution that allows for both "where" and "how" systems that are functionally and structurally organized within the posterior parietal lobe.     

Domain specificity in the primate prefrontal cortex

Experimental studies in nonhuman primates and functional imaging studies in humans have underlined the critical role played by the prefrontal cortex (PFC) in working memory. However, the precise organization of the frontal lobes with respect to the different types of information operated upon is a point of controversy, and several models of functional organizations have been proposed. One model, developed by Goldman-Rakic and colleagues, postulates a modular organization of working memory based on the type of information processing (the domain specificity hypothesis). Evidence to date has focused on the encoding of the locations of visual objects by the dorsolateral PFC, whereas the ventrolateral PFC is suggested to be involved in processing the features and identity of objects. In this model, domain should refer to any sensory modality that registers information relevant to that domain—for example, there would be visual and auditory input to a spatial information processing region and a feature analysis system. In support of this model, recent studies have described pathways from the posterior and anterior auditory association cortex that target dorsolateral spatial-processing regions and ventrolateral object-processing regions, respectively. In addition, physiological recordings from the ventrolateral PFC indicate that some cells in this region are responsive to the features of complex sounds. Finally, recordings in adjacent ventrolateral prefrontal regions have shown that the features of somatosensory stimuli can be discriminated and encoded by ventrolateral prefrontal neurons. These discoveries argue that two domains, differing with respect to the type of information being processed, and not with respect to the sensory modality of the information, are specifically localized to discrete regions of the PFC and embody the domain specificity hypothesis, first proposed by Patricia Goldman-Rakic.     

Integrating faces, houses, motion, and action: spontaneous binding across ventral and dorsal processing streams

Perceiving an event requires the integration of its features across numerous brain maps and modules. Visual object perception is thought to be mediated by a ventral processing stream running from occipital to inferotemporal cortex, whereas most spatial processing and action control is attributed to the dorsal stream connecting occipital, parietal, and frontal cortex. Here we show that integration operates not only on ventral features and objects, such as faces and houses, but also across ventral and dorsal pathways, binding faces and houses to motion and manual action. Furthermore, these bindings seem to persist over time, as they influenced performance on future task-relevant visual stimuli. This is reflected by longer reaction times for repeating one, but alternating other features in a sequence, compared to complete repetition or alternation of features. Our findings are inconsistent with the notion that the dorsal stream is operating exclusively online and has no access to memory.     

Central visual persistences: II. Effects of hand and head rotations

In an earlier paper, kinesthetic effects on central visual persistences (CPs) were reported, including the ability to move these images by hand following eye closure. While all CPs could be translated anywhere within the frontal field, the present report documents a more selective influence of manual rotations on CPs in the same subjects. When common objects or figures drawn on cards were rotated (while holding one end of the object or one corner of a card between thumb and forefinger), it was found that CPs of larger objects rotated with the hand. By contrast, CPs of smaller objects, parts of objects, and textures remained stable in space as the hand rotated. It is proposed that CPs of smaller stimuli and textures are represented mainly by the ventral stream (temporal cortex) while larger CPs, which rotate, are represented mainly by the dorsal stream (parietal cortex). A second discovery was that CPs of small objects (but not of line segments or textures) could be rotated when the thumb and fingers surrounded the edges of the object. It is proposed that neuronal convergence of visual and tactile information about shape increases parietal responses to small objects, so that their CPs will rotate. Experiments with CPs offer new tools to infer visual coding differences between ventral and dorsal streams in man.     

Cortical dynamics of contextually cued attentive visual learning and search: spatial and object evidence accumulation

How do humans use target-predictive contextual information to facilitate visual search? How are consistently paired scenic objects and positions learned and used to more efficiently guide search in familiar scenes? For example, humans can learn that a certain combination of objects may define a context for a kitchen and trigger a more efficient search for a typical object, such as a sink, in that context. The ARTSCENE Search model is developed to illustrate the neural mechanisms of such memory-based context learning and guidance and to explain challenging behavioral data on positive-negative, spatial-object, and local-distant cueing effects during visual search, as well as related neuroanatomical, neurophysiological, and neuroimaging data. The model proposes how global scene layout at a first glance rapidly forms a hypothesis about the target location. This hypothesis is then incrementally refined as a scene is scanned with saccadic eye movements. The model simulates the interactive dynamics of object and spatial contextual cueing and attention in the cortical What and Where streams starting from early visual areas through medial temporal lobe to prefrontal cortex. After learning, model dorsolateral prefrontal cortex (area 46) primes possible target locations in posterior parietal cortex based on goal-modulated percepts of spatial scene gist that are represented in parahippocampal cortex. Model ventral prefrontal cortex (area 47/12) primes possible target identities in inferior temporal cortex based on the history of viewed objects represented in perirhinal cortex.     

The role of spatial configuration in tests of working memory explored with functional neuroimaging

While the importance of the prefrontal cortex for "higher-order" cognitive functions is largely undisputed, no consensus has been reached regarding the fractionation of functions within this region. Several recent functional neuroimaging studies have suggested that the mid-ventrolateral frontal cortex may play an important role in various aspects of human memory. Thus, similar patterns of activation have been observed in this region during analogous spatial, verbal and visual span tasks. In the present study, however, activation was observed in a more dorsolateral region of the lateral frontal cortex during a modified version of the spatial span task, which differed only in the spatial configuration of the array employed. The results of a supplementary behavioral study, designed to investigate this effect further, suggest that in spatial memory tasks certain stimulus configurations may encourage subjects to adopt mnemonic strategies, which may depend upon dorsolateral, rather than ventrolateral, regions of the frontal cortex. These findings shed further light on the functional relationship between dorsal and ventral regions of the lateral frontal cortex and, more specifically, how the "executive" processes assumed to be dependent upon these regions might contribute to aspects of human memory.     

Spatial and nonspatial working memory and visual search

It has been indicated that visual search is interfered with in spatial working memory (WM), although not in nonspatial WM. In this study, the effects on visual search of individual differences in spatial and nonspatial WM were examined. Two visual search conditions were used: a conjunction search condition comprising two features (color and shape) and a disjunction condition comprising only one feature (color or shape). 96 participants (42 men, 54 women, M age = 20.9 yr., SD = 3.5) participated in this study. The participants were divided into high and low WM groups based on their spatial and nonspatial WM test scores. As a result, statistically significant group differences in the conjunction search rate were observed in spatial WM but not in nonspatial WM. These results suggest there is a relationship between visual search and the individual spatial WM ability, but this does not hold for nonspatial WM.     

Brain activation and deactivation during location and color working memory tasks in 11-13-year-old children

Using functional magnetic resonance imaging (fMRI) and n-back tasks we investigated whether, in 11-13-year-old children, spatial (location) and nonspatial (color) information is differentially processed during visual attention (0-back) and working memory (WM) (2-back) tasks and whether such cognitive task performance, compared to a resting state, results in regional deactivation. The location 0-back task, compared to the color 0-back task, activated segregated areas in the frontal, parietal and occipital cortices whereas no differentially activated voxels were obtained when location and color 2-back tasks were directly contrasted. Several midline cortical areas were less active during 0- and 2-back task performance than resting state. The task-induced deactivation increased with task difficulty as demonstrated by larger deactivation during 2-back than 0-back tasks. The results suggest that, in 11-13-year-old children, the visual attentional network is differently recruited by spatial and nonspatial information processing, but the functional organization of cortical activation in WM in this age group is not based on the type of information processed. Furthermore, 11-13-year-old children exhibited a similar pattern of cortical deactivation that has been reported in adults during cognitive task performance compared to a resting state.     

Maintenance versus manipulation of information held in working memory: an event-related fMRI study.

One model of the functional organization of lateral prefrontal cortex (PFC) in primates posits that this region is organized in a dorsal/ventral fashion subserving spatial and object working memory, respectively. Alternatively, it has been proposed that a dorsal/ventral subdivision of lateral PFC instead reflects the type of processing performed upon information held in working memory. We tested this hypothesis using an event-related fMRI method that can discriminate among functional changes occurring during temporally separated behavioral subcomponents of a single trial. Subjects performed a delayed-response task with two types of trials in which they were required to: (1) retain a sequence of letters across the delay period (maintenance) or (2) reorder the sequence into alphabetical order across the delay period (manipulation). In each subject, activity during the delay period was found in both dorsolateral and ventrolateral PFC in both types of trials. However, dorsolateral PFC activity was greater in manipulation trials. These findings are consistent with the processing model of the functional organization of working memory in PFC.     

A right visual field advantage for visual processing of manipulable objects

Information about object-associated manipulations is lateralized to left parietal regions, while information about the visual form of tools is represented bilaterally in ventral occipito-temporal cortex. It is unknown how lateralization of motor-relevant information in left-hemisphere dorsal stream regions may affect the visual processing of manipulable objects. We used a lateralized masked priming paradigm to test for a right visual field (RVF) advantage in tool processing. Target stimuli were tools and animals, and briefly presented primes were identical to or scrambled versions of the targets. In Experiment 1, primes were presented either to the left or to the right of the centrally presented target, while in Experiment 2, primes were presented in one of eight locations arranged radially around the target. In both experiments, there was a RVF advantage in priming effects for tool but not for animal targets. Control experiments showed that participants were at chance for matching the identity of the lateralized primes in a picture?Cword matching experiment and also ruled out a general RVF speed-of-processing advantage for tool images. These results indicate that the overrepresentation of tool knowledge in the left hemisphere affects visual object recognition and suggests that interactions between the dorsal and ventral streams occurs during object categorization.     

Age differences in prefrontal cortical activity in working memory

Working memory (WM) declines with advancing age. Brain imaging studies indicate that ventral prefrontal cortex (PFC) is active when information is retained in WM and that dorsal PFC is further activated for retention of large amounts of information. The authors examined the effect of aging on activation in specific PFC regions during WM performance. Six younger and 6 older adults performed a task in which, on each trial, they (a) encoded a 1- or 6-letter memory set, (b) maintained these letters over 5-s. and (c) determined whether or not a probe letter was part of the memory set. Comparisons of activation between the 1- and 6-letter conditions indicated age-equivalent ventral PFC activation. Younger adults showed greater dorsal PFC activation than older adults. Older adults showed greater rostral PFC activation than younger adults. Aging may affect dorsal PFC brain regions that are important for WM executive components.     

Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information

Working memory for names and faces was investigated to ascertain whether verbal and nonspatial visual information is maintained in working memory by separate neural systems. The subjects performed a delayed match-to-sample task for famous or unfamous faces and names and a sensorimotor control task. Several occipital, temporal, parietal, and prefrontal areas were activated during all memory delays, in comparison with the control delays. Greater delay activity for unfamous faces than for names was obtained in the right fusiform gyrus, right inferior frontal gyrus (IFG), right IFG/ precentral gyrus, and right medial superior frontal gyrus, whereas greater delay activity for unfamous names than for faces was observed in the precuneus, left insula/postcentral gyrus, and left IFG/ precentral gyrus. There was no significant difference in the prefrontal activity in the comparison between famous faces and names. Greater delay activity for famous names than for faces was obtained in visual association and parietal areas. The results indicate that there is a functional dissociation based on information type within the neural system that is responsible for working memory maintenance of verbal and nonspatial visual information.     

The hare and the snail: Dissociating visual orienting from conscious perception

A method for investigating attentional effects of peripheral visual objects, independently of perceptual identification, is described. We report an experiment using this method which shows that visual processing of peripheral objects differs radically, depending on whether participants move attention in response to an object or consciously perceive that object. When luminance contrast was reduced, conscious perceptual discrimination of peripheral letters was massively slower and less accurate—but both low and high contrast letters elicited rapid attentional orienting effects and these rapid orienting effects were equal in magnitude across low and high contrast. This pattern is consistent with known differences in luminance sensitivity between the dorsal and ventral visual processing streams, and with rapid dorsal–ventral interaction mediated via re-entrant feedback. Our findings show that the control system responsible for rapid movements of attention is exquisitely sensitive to visual form information at low levels of contrast, and involves a different neurocognitive pathway to that which gives rise to conscious perception.     

Interactions between the dorsal and the ventral pathways in mental rotation: An fMRI study

In this fMRI study, we examined the relationship between activations in the inferotemporal region (ventral pathway) and the parietal region (dorsal pathway), as well as in the prefrontal cortex (associated with working memory), in a modified mental rotation task. We manipulated figural complexity (simple vs. complex) to affect the figure recognition process (associated with the ventral pathway) and the amount of rotation (0° vs. 90°), typically associated with the dorsal pathway. The pattern of activation not only showed that both streams are affected by both manipulations, but also showed an overadditive interaction. The effect of figural complexity was greater for 90° rotation than for 0° in multiple regions, including the ventral, dorsal, and prefrontal regions. In addition, functional connectivity analyses on the correlations across the time courses of activation between regions of interest showed increased synchronization among multiple brain areas as task demand increased. The results indicate that both the dorsal and the ventral pathways show interactive effects of object and spatial processing, and they suggest that multiple regions interact to perform mental rotation.     

Modality and domain specific components in auditory and visual working memory tasks

In the tripartite model of working memory (WM) it is postulated that a unique part system—the visuo-spatial sketchpad (VSSP)—processes non-verbal content. Due to behavioral and neurophysiological findings, the VSSP was later subdivided into visual object and visual spatial processing, the former representing objects’ appearance and the latter spatial information. This distinction is well supported. However, a challenge to this model is the question how spatial information from non-visual sensory modalities, for example the auditory one, is processed. Only a few studies so far have directly compared visual and auditory spatial WM. They suggest that the distinction of two processing domains—one for object and one for spatial information—also holds true for auditory WM, but that only a part of the processes is modality specific. We propose that processing in the object domain (the item’s appearance) is modality specific, while spatial WM as well as object-location binding relies on modality general processes.     

The privileged role of location in visual working memory

Reports have conflicted about the possible special role of location in visual working memory (WM). One important question is: Do we maintain the locations of objects in WM even when they are irrelevant to the task at hand? Here we used a continuous response scale to study the types of reporting errors that participants make when objects are presented at the same or at different locations in space. When several objects successively shared the same location, participants exhibited a higher tendency to report features of the wrong object in memory; that is, they responded with features that belonged to objects retained in memory but not probed at retrieval. On the other hand, a similar effect was not observed when objects shared a nonspatial feature, such as color. Furthermore, the effect of location on reporting errors was present even when its manipulation was orthogonal to the task at hand. These findings are consistent with the view that binding together different nonspatial features of an object in memory might be mediated through an object’s location. Hence, spatial location may have a privileged role in WM. The relevance of these findings to conceptual models, as well as to neural accounts of visual WM, is discussed.     

The effect of spatial and nonspatial contextual information on visual object memory

Recent research has found visual object memory can be stored as part of a larger scene representation rather than independently of scene context. The present study examined how spatial and nonspatial contextual information modulate visual object memory. Two experiments tested participants’ visual memory by using a change detection task in which a target object's orientation was either the same as it appeared during initial viewing or changed. In addition, we examined the effect of spatial and nonspatial contextual manipulations on change detection performance. The results revealed that visual object representations can be maintained reliably after viewing arrays of objects. Moreover, change detection performance was significantly higher when either spatial or nonspatial contextual information remained the same in the test image. We concluded that while processing complex visual stimuli such as object arrays, visual object memory can be stored as part of a comprehensive scene representation, and both spatial and nonspatial contextual changes modulate visual memory retrieval and comparison.     

Dorsal and ventral visual streams: Typical and atypical development

The literature on visuospatial processing describes two distinct pathways within the brain: a dorsal route extending from the visual cortex into the parietal lobes that is critical for spatial processing and a ventral route extending from the visual cortex into the temporal lobes that is critical for form perception. These visual streams appear to differ in their developmental trajectories and their vulnerabilities to diverse neurodevelopmental conditions. The present work aims to investigate development and vulnerability in two aspects of dorsal and ventral visual-stream function, namely attention to location and attention to identity. In Study 1, we compare typically-developing (TD) youth aged 9 to 16 years with young adults aged 18 to 22 years on computerized location and identity tasks. In Study 2, we compare children and adolescents who have congenital hypothyroidism (CH), a pediatric endocrine disorder, with age-matched TD controls on the same tasks. The results from Study 1 show that the youths were less accurate than the adults at judging identity, whereas both groups were equally accurate at judging location. The results from Study 2 show that the youths with CH were slower but not less accurate than the TD youths in making both identity and location judgments. The results are interpreted as signifying later development of ventral (identity) stream functions compared to dorsal (location) but equal vulnerability of both functions in CH.