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Working memory for visual objects: complementary roles of inferior temporal, medial temporal, and prefrontal cortex.

Humans have an extraordinary ability to maintain and manipulate visual image information in the absence of perceptual stimulation. The neural substrates of visual working memory have been extensively researched, but there have been few attempts to integrate these findings into a model of how different cortical areas interact to form and maintain visual memories. In this paper, I review findings from neurophysiological, neuropsychological, and neuroimaging studies of visual working memory in human and nonhuman primates. These data support a model in which visual working memory operations rely on activation of object representations in inferior temporal cortex, via top-down feedback from neocortical areas in the prefrontal and medial temporal cortex, and also from the hippocampus.

Animals↗

Assessing the working memory network: studies with functional magnetic resonance imaging and structural equation modeling.

A considerable body of evidence supports the notion that the neurofunctional substrate of working memory is not only related to the integrity of the prefrontal cortex, but also to the concerted interplay of widespread interacting networks including the parietal cortex, subcortical regions and cerebellar areas. Modern functional brain imaging techniques such as functional magnetic resonance imaging (fMRI) have provided a detailed picture of functional neuroanatomy subserving working memory functions. Most of the earlier functional studies were directed toward the identification of brain areas subserving specific cognitive domains in terms of a functional segregation. More recently, different multivariate techniques were employed to specifically address measures of functional or effective connectivity. Structural equation modeling (SEM) or path analysis is one of the most often used methods to model interactions among covarying brain areas in an explicitly model-based approach. The present review will focus on basic methodological issues of SEM for the analysis of fMRI datasets in studies of working memory. Aside from a discussion of previous studies and their essential findings, advanced methodological issues and caveats as well as future perspectives of the method will be addressed.

Brain↗

Impaired discourse gist and working memory in children after brain injury.

Emerging evidence suggests that a traumatic brain injury (TBI) in childhood may disrupt the ability to abstract the central meaning or gist-based memory from connected language (discourse). The current study adopts a novel approach to elucidate the role of immediate and working memory processes in producing a cohesive and coherent gist-based text in the form of a summary in children with mild and severe TBI as compared to typically developing children, ages 8-14 years at test. Both TBI groups showed decreased performance on a summary production task as well as retrieval of specific content from a long narrative. Working memory on n-back tasks was also impaired in children with severe TBI, whereas immediate memory performance for recall of a simple word list in both TBI groups was comparable to controls. Interestingly, working memory, but not simple immediate memory for a word list, was significantly correlated with summarization ability and ability to recall discourse content.

Adolescent↗

Theta oscillations in human cortex during a working-memory task: evidence for local generators.

Cortical theta appears important in sensory processing and memory. Intracanial electrode recordings provide a high spatial resolution method for studying such oscillations during cognitive tasks. Recent work revealed sites at which oscillations in the theta range (4-12 Hz) could be gated by a working-memory task: theta power was increased at task onset and continued until task offset. Using a large data set that has now been collected (10 participants/619 recording sites), we have sufficient sampling to determine how these gated sites are distributed in the cortex and how they are synchronized. A substantial fraction of sites in occipital/parietal (45/157) and temporal (23/280) cortices were gated by the task. Surprisingly, this aspect of working-memory function was virtually absent in frontal cortex (2/182). Coherence measures were used to analyze the synchronization of oscillations. We suspected that because of their coordinate regulation by the working-memory task, gated sites would have synchronized theta oscillations. We found that, whereas nearby gated sites (<20 mm) were often but not always coherent, distant gated sites were almost never coherent. Our results imply that there are local mechanisms for the generation of cortical theta.

Adolescent↗

Functional disconnection between the prefrontal and parietal cortices during working memory processing in schizophrenia: a[15(O)]H2O PET study.

OBJECTIVE: The prefrontal-parietal circuits have been reported to play an important role in working memory. The purpose of this study was to use direct neuroimaging to address whether interregional correlation in the prefrontal-parietal circuits is impaired in schizophrenia. METHOD: [(15)O]H(2)O positron emission tomography was used to compare regional blood flow changes in 12 schizophrenic and 12 healthy comparison subjects during the n-back sequential-picture working memory task. Interregional correlation was assessed by correlating the regional activation of the lateral prefrontal area with that of other activated areas in each subject group. RESULTS: Dorsolateral prefrontal activation was observed around the right superior frontal sulcus in the healthy subjects, and ventrolateral prefrontal activation below the right inferior frontal sulcus was observed in the schizophrenic patients. Activation in the right lateral prefrontal cortex was significantly correlated with activation in the bilateral inferior parietal region in the healthy subjects but was not correlated with any regional activation in the patients. CONCLUSIONS: The findings suggest prefrontal-parietal functional disconnection, particularly prefrontal dissociation and abnormal prefrontal-parietal interaction, during working memory processing in schizophrenia.

Adult↗

Level of response to alcohol and brain response during visual working memory.

OBJECTIVE: This study examined neural correlates of the low level of response to alcohol using functional magnetic resonance imaging (FMRI) during a challenging visual working memory task. METHOD: Participants were healthy adolescents (N = 35) with a range of drinking patterns recruited from local high schools. After a minimum 5 days of abstinence from alcohol and other drugs, FMRI, neuropsychological testing and the Self-Rating of the Effects of Alcohol were administered. RESULTS: Self-report of initial level of response to alcohol was significantly predicted by FMRI blood oxygen level dependent (BOLD) response to the visual working memory task in the right prefrontal and bilateral anterior cingulate region (12% of unique variance, p < .05) and right cerebellum and parahippocampal gyrus (17% of unique variance, p < .01), above and beyond effects accounted for by drinks consumed per month, age, gender and ethnicity. CONCLUSIONS: Young people who report having needed more alcohol to achieve specific effects during early drinking experiences show higher levels of brain response during visual working memory, perhaps suggesting less capacity to adjust cognitive processing to contextual demands.

Adolescent↗

Complexity effects in visuo-spatial working memory: implications for the role of long-term memory.

Several studies have shown that the capacity of visuo-spatial working memory is limited by complexity. Using a variant of the Corsi blocks task, this paper investigates the effect of complexity of the to-be-remembered path on visuo-spatial memory span. Redundancy was determined by three Gestalt principles: symmetry, repetition, and continuation. Experiment 1 revealed an effect of path complexity. The subsequent experiments explored whether the superiority for recall of structured over complex paths can be attributed solely to the operation of visuo-spatial working memory, or whether it also reflects the use of long-term knowledge. Experiment 2 demonstrated that the effect of complexity remained, even when the mechanisms for visuo-spatial coding were removed by a secondary visuo-spatial task. In Experiments 3 and 4 subjects were trained in the recall of complex paths. This led to the creation of long-term memory representations for these paths, as shown by an improvement in their span, and a concomitant lack of transfer to new paths. Finally, Experiment 5 showed that one prior repetition of a complex path was sufficient to produce specific and long-term learning effects. These results point to the involvement of long-term memory processes in the temporary retention of visuo-spatial material for which representations exist in long-term memory. They also suggest that the effect of complexity may provide a tractable technique for investigating the mechanisms underlying the limits of visuo-spatial short-term storage.

Humans↗

Arithmetic operation and working memory: differential suppression in dual tasks.

The relationship between arithmetic function and working memory was examined using a dual-task paradigm for either phonological or visuo-spatial suppression. Simultaneous phonological rehearsal significantly delayed the performance of multiplication but not subtraction, whereas holding an image in the mind delayed subtraction but not multiplication. This result indicates that arithmetic function is related to working memory in a subsystem-specific manner: multiplication is more closely linked to phonological loop and subtraction to visuo-spatial sketchpad. Whereas this is not compatible with the notion that arithmetic is done on a unitary, amodal representation of numbers, it provides support for the triple-code and/or the modular processing models on human numerical cognition in which number representations are specific for input/output modality and arithmetic types.

Adult↗

Demand on verbal working memory delays haemodynamic response in the inferior prefrontal cortex.

Event-related functional magnetic resonance imaging was used to test the involvement of the inferior prefrontal cortex in verbal working memory. Pairs of French nouns were presented to ten native French speakers who had to make semantic or grammatical gender decisions. Verbal working memory involvement was manipulated by making the categorization of the second noun optional. Decisions could be made after processing the first noun only (RELEASE condition) or after processing the two nouns (HOLD condition). Reaction times suggested faster processing for gender than for semantic category in RELEASE. Despite the absence of anatomical difference across tasks and conditions in the wide activated network, the haemodynamic response peak latencies of the inferior prefrontal cortex were significantly delayed in HOLD versus RELEASE while no such peak delay was observed in the superior temporal gyrus. Interestingly, this pattern did not interact with language tasks. This study shows that cognitive manipulation can influence haemodynamic time-course and suggests that the main cognitive process determining inferior prefrontal activation is verbal working memory rather than specific linguistic processes such as grammatical or semantic analysis.

Acoustic Stimulation↗

Comparison between the effects of ethanol and diazepam on spatial working memory in the rat.

The present study compared the effects of ethanol and diazepam on a task that allows for the assessment of both spatial working memory and the acquisition of spatial information within each day. During the first trial of each day, subjects were shown the spatial location of a food reward on a six-arm radial-arm maze. During nine subsequent free-choice trials, subjects were reinforced for returning to that same spatial location. The location of the food reward varied across days. Thus, choosing correctly on any given trial required subjects to remember where food had been received during the previous trials of that day. The effects of ethanol and diazepam on working memory were assessed by analyzing the overall number of errors committed during the nine free-choice trials of each day. The effects of ethanol and diazepam on within-day acquisition were assessed by comparing the number of errors committed during the first three trials of each day to the number of errors committed during the last three trials of each day. Ethanol and diazepam both produced dose-dependent increases in working memory errors, and both did so without impairing within-day acquisition. The results of the present study provide further evidence of the similarities between the effects of ethanol and benzodiazepine receptor agonists on learning and memory, and are consistent with the hypothesis that ethanol's potentiation of GABA at GABAA receptors contributes to the learning and memory impairments produced by ethanol.

Adaptation, Psychological↗

Interference resolution in spatial working memory.

Anterior cingulate and lateral inferior prefrontal cortex (PFC) are considered important for conflict monitoring and interference resolution in many verbal tasks. We studied interference resolution in a spatial working memory task using event-related fMRI. The task required participants to ignore two locations from a set of four initially held in working memory and to remember the remaining two locations as the target set for a subsequent recognition test. Familiarity of nontarget probes was manipulated by drawing the probe from either the ignored locations [high familiarity (HF)] or locations not used in the present trial [low familiarity (LF)]. Precentral sulcus (PrCS) and superior parietal lobe (SPL), two regions commonly associated with motor planning and spatial attention, showed heightened activity in response to increased level of interference from nontargets of high familiarity. Our finding suggests that interference resolution in the spatial domain may involve a different subset of the working memory system from that in the verbal domain.

Adult↗

A visuospatial "phonological loop" in working memory: evidence from American Sign Language.

In two experiments, the question of whether working memory could support an articulatory rehearsal loop in the visuospatial domain was investigated. Deaf subjects fluent in American Sign Language (ASL) were tested on immediate serial recall. In Experiment 1, with ASL stimuli, evidence was found for manual motoric coding (worse recall under articulatory suppression) and previous findings of ASL-based phonological coding (worse recall for phonologically similar lists) were replicated [corrected]. The two effects did not interact, suggesting separate components which both contribute to performance. Stimuli in Experiment 2 were namable pictures, which had to be recoded for ASL-based rehearsal to occur. Under these conditions, articulatory suppression eliminated the phonological similarity effect. Thus, an articulatory process seems to be used in translating pictures into a phonological code for memory maintenance. These results indicate a configuration of components similar to the phonological loop for speech, suggesting that working memory can develop a language-based rehearsal loop in the visuospatial modality.

Adolescent↗

Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: results From the National Institute of Mental Health's BIOCARD study.

The cognitive consequences of the apolipoprotein E-epsilon4 (APOE-epsilon4) allele were examined in middle age, before likely onset of symptoms of Alzheimer's disease. The authors identified 3 cognitive processes--visuospatial attention, spatial working memory, and the effect of visuospatial attention on working memory--and devised "behavioral assays" of the integrity of components of these processes. Redirecting visuospatial attention, retention of memory for location, and attentional modulation of memory of target location were affected by APOE genotype. Visuospatial attention showed additive effects of epsilon4 gene dose; each additional epsilon4 allele inherited further slowed disengagement from invalidly cued space. In contrast, working memory performance was affected only in epsilon4 homozygotes. Effect sizes for the APOE gene were moderate to large, ranging from 14% to 24%. Effects of APOE genotype on component processes of cognition in healthy, middle-aged adults is consistent with the emergence in adulthood of an APOE-epsilon4 cognitive phenotype.

Adult↗

Preliminary study of working memory in children with stroke related to sickle cell disease.

The verbal working memory abilities of children with stroke related to sickle cell disease (SCD) (n = 20) were compared to those of control children with SCD who had no history of stroke (n = 11). Memory span for one-, two-, and three-syllable words was assessed. For children with anterior infarcts, overall span was comparable to that of controls, but the typical effect of word length on span was reduced. For children with diffuse infarcts, overall span was reduced in comparison to that of controls, but the typical effect of word length on span was observed. For children with posterior infarcts, overall span was comparable to that of controls and the typical effect of word length on span was observed. These results provide preliminary evidence that patterns of working memory performance may vary across children with infarcts affecting different regions of the brain.

Adolescent↗

Spatial and object working memory impairments in schizophrenia patients: a Bayesian item-response theory analysis.

This study reports evidence that schizophrenia patients are significantly impaired in both spatial and object (shape) working memory. A 3-s delay between exposure and recall of targets was used and Bayesian item-response theory was applied to compensate for the tasks' differential difficulty while simultaneously taking account of missing data from participant attrition. Weaker evidence was found that in schizophrenia both domains are equally impaired on average, that spatial and object working memory appear to be more highly correlated with each other in the schizophrenia population than in the normal population, and that schizophrenia patients show greater variability in spatial than object working memory performance.

Adult↗

The functional organization of working memory processes within human lateral frontal cortex: the contribution of functional neuroimaging.

Recent functional neuroimaging studies have provided a wealth of new information about the likely organization of working memory processes within the human lateral frontal cortex. This article seeks to evaluate the results of these studies in the context of two contrasting theoretical models of lateral frontal-lobe function, developed through lesion and electrophysiological recording work in non-human primates (Goldman-Rakic, 1994, 1995; Petrides, 1994, 1995). Both models focus on a broadly similar distinction between anatomically and cytoarchitectonically distinct dorsolateral and ventrolateral frontal cortical areas, but differ in the precise functions ascribed to those regions. Following a review of the relevant anatomical data, the origins of these two theoretical positions are considered in some detail and the main predictions arising from each are identified. Recent functional neuroimaging studies of working memory processes are then critically reviewed in order to assess the extent to which they support either, or both, sets of predictions. The results of this meta-analysis suggest that lateral regions of the frontal lobe are not functionally organized according to stimulus modality, as has been widely assumed, but that specific regions within the dorsolateral or ventrolateral frontal cortex make identical functional contributions to both spatial and non-spatial working memory.

Animals↗

Intrusion errors in visuospatial working memory performance.

This study tested the hypothesis that failure in active visuospatial working memory tasks involves a difficulty in avoiding intrusions due to information that is already activated. Two experiments are described, in which participants were required to process several series of locations on a 4 x 4 matrix and then to produce only the final location of each series. Results revealed a higher number of errors due to already activated locations (intrusions) compared with errors due to new locations (inventions). Moreover, when participants were required to pay extra attention to some irrelevant (non-final) locations by tapping on the table, intrusion errors increased. Results are discussed in terms of current models of working memory functioning.

Adolescent↗

Distributing working memory resources during problem solving.

This study examines how problem solvers distribute working memory demands over internal and external resources. Participants recorded notes while performing an arithmetic task. They recorded a majority of intermediate results and labeled many of those results (e.g., "C = 10"). When more effort was required to take notes, participants recorded fewer results. Participants with a consistent goal structure recorded fewer results and with practice labeled fewer recorded results than those with varied goal structures. When notes were displayed in a consistent spatial arrangement participants labeled fewer recorded results than when notes appeared in varied locations. These findings indicate that individuals use explicit and implicit strategies for indexing intermediate results. The data support the view that individuals flexibly distribute working memory over internal and external resources in response to situational cost-benefit considerations.

Adult↗