Faculty | Neuroscience special issue
Neuroscience special issue on
Cognitive Neuroscience of Working Memory
Guest Editors
Grega Repovš, Maja Bresjanac
Background
In recent years, multidisciplinary research within cognitive neuroscience has established itself as a promising approach to answering the question of how the mind emerges from the working of the brain. One of the fields that has gained substantially by successfully combining the theoretical frameworks, methodologies, empirical results and insights of the varied disciplines within cognitive neuroscience, is the study of working memory. Today we are able to describe the functional properties of the working memory and its subsystems, we are identifying the brain regions involved in the storage and manipulation of information in working memory, and are starting to understand the functional networks that they form, we are gaining understanding of the neuronal representational codes and the roles of respective neurotransmitters, we are building computer simulations that could enable us to understand and predict the complex mechanisms involved. More than ever, the interdisciplinary collaboration could provide us with new major insights into this important cognitive ability.
The aim of this special issue is to present the state-of-the-art in the cognitive neuroscience of working memory and to foster further efforts in developing interdisciplinary research, as well as interdisciplinary exchange of ideas and findings. The aim of the issue is to address a wide variety of research questions within the field, including - but not limited - to:
- What are the properties, capabilities and limitations of working memory?
- What can we learn of working memory from its dysfunctions?
- What are the cortical areas and the neural activity related to working memory?
- What are the molecular/cellular bases of working memory?
- What can computer models and simulations reveal about the working memory?
The Neuroscience special issue on working memory is structured in three parts. The first two parts consist of invited review papers from prominent researchers in the field, while the third part presents empirical papers that were contributed through an open call for papers. The emphasis throughout the issue is on interdisciplinary exchange of ideas and strategies of solving the outlined research questions.
Cognitive Neuroscience of Working Memory: A Prologue
Grega Repovš, Maja Bresjanac
The paper provides a rationale and an overview of the issue. It introduces the subject of working memory and presents a multidisciplinary research framework that can be used to develop comprehensive theories and models of human cognition. The framework, promoting iterative and interactive combination of methods and insights provided by individual disciplines, served as the backbone on which the issue was built.
Part I: What is working memory and how can we study it?
The aim of the first part is to present the ways in which different cognitive neurosciences approach the study of working memory. It presents their basic assumptions and theoretical background, research methods, core / recent insights and the ways in which they relate to, offer and use insights from other sciences in relation to working memory.
The multi-component model of working memory: explorations in experimental cognitive psychology
Grega Repovš, Alan Baddeley
There are a number of ways one can hope to describe and explain cognitive abilities, each of them contributing a unique and valuable perspective. Cognitive psychology tries to develop and test functional accounts of cognitive systems that explain the capacities and properties of cognitive abilities as revealed by empirical data gathered by a range of behavioral experimental paradigms. Much of the research in the cognitive psychology of working memory has been strongly influenced by the multi-component model of working memory (Baddeley and Hitch, 1974; Baddeley, 1986, 2000, in press). By expanding the notion of a passive short-term memory to an active system that provides the basis for complex cognitive abilities, the model has opened up numerous questions and new lines of research. In this paper we present the current revision of the multi-component model that encompasses a central executive, two unimodal storage systems: a phonological loop and a visuospatial sketchpad, and a further component, a multimodal store capable of integrating information into unitary episodic representations, termed episodic buffer. We review recent empirical data within experimental cognitive psychology that has shaped the development of the multicomponent model and the understanding of the capacities and properties of working memory. Research based largely on dual-task experimental designs and on neuropsychological evidence has yielded valuable information about the fractionation of working memory into independent stores and processes, the nature of representations in individual stores, the mechanisms of their maintenance and manipulation, the way the components of working memory relate to each other, and the role they play in other cognitive abilities. With many questions still open and new issues emerging, we believe that the multicomponent model will continue to stimulate research while providing a comprehensive functional description of working memory.
Working Memory as an Emergent Property of the Mind and Brain
Bradley R. Postle
Cognitive neuroscience research on working memory has been largely motivated by a standard model that arose from the melding of psychological theory with neuroscience data. Among the tenets of this standard model are that working memory functions arise from the operation of specialized systems that act as buffers for the storage and manipulation of information, and that frontal cortex (particularly prefrontal cortex) is a critical neural mb_substrate for these specialized systems. However, the standard model has been a victim of its own success, and can no longer accommodate many of the empirical findings of studies that it has motivated. An alternative is proposed: Working memory functions arise through the coordinated recruitment, via attention, of brain systems that have evolved to accomplish sensory-, representation-, and action-related functions. Evidence from behavioral, neuropsychological, electrophysiological, and neuroimaging studies, from monkeys and humans, is considered, as is the question of how to interpret delay-period activity in the prefrontal cortex.
Individual differences in working memory
Chris Jarrold, John N. Towse
Working memory can be defined as the ability to hold in mind information in the face of potentially interfering distraction in order to guide behaviour. The experimental manipulation of working memory tasks has shed considerable light on the probable structure of the human working memory system, and, to a lesser extent, the specific processes captured by working memory paradigms. However, individual differences research has also had a crucial role to play in the development of theories of working memory. In particular, correlational approaches have been particularly informative in three areas of working memory research, each of which is reviewed here. These are, first, the importance of working memory measures as correlates of high-level cognitive skills such as reading, mathematics, reasoning, and fluid intelligence; second, the extent to which human working memory relies on domain-general or domain-specific component subsystems, and third, the precise reasons why working memory measures do relate to other important indices of human cognitive functioning. The findings from each of these areas suggest that working memory depends on a combination of domain- specific representational systems and domain-general processing and control systems, and that working memory measures capture individuals' ability to combine maintenance and processing demands in a manner that limits information loss from forgetting or distraction.
The functional neuroanatomy of working memory - contributions of human brain lesion studies
Notger G. Mëźller, Robert T. Knight
Studies of patients with focal brain lesions remain critical components of research programs attempting to understand human brain function. Whereas functional imaging typically reveals activity in distributed brain regions that are involved in a task, lesion studies can define which of these brain regions are necessary for a cognitive process. Further, lesion studies are less critical regarding the selection of baseline conditions needed in functional brain imaging research. Lesion studies suggest a functional subdivision of the visuospatial sketchpad of working memory (WM) with a ventral stream reaching from occipital to temporal cortex supporting object recognition and a dorsal stream connecting the occipital with parietal cortex enabling spatial operations. The phonological loop can be divided into a phonological short-term store in inferior parietal cortex and an articulatory subvocal rehearsal process relying on brain areas necessary for speech production, i.e., Broca's area, the supplementary motor association area (SMA) and possibly the cerebellum.
More uncertainty exists regarding the role of the prefrontal cortex (PFC) in WM. Whereas single cell studies in non-human primates and functional imaging studies in humans have suggested an extension of the ventral and dorsal path into different subregions of the PFC, lesion studies together with recent single-cell and imaging studies point to a non-mnemonic role of the PFC, including attentional control of sensory processing, integration of information from different domains, stimulus selection and monitoring of information held in memory. Our own data argue against a modulatory view of the PFC and suggest that processes supporting WM are distributed along ventral and dorsal lateral PFC.
Investigating principles of human brain function underlying working memory: what insights from schizophrenia?
Garry Honey, Paul C. Fletcher
Working memory dysfunction is a core component of schizophrenia, which likely contributes substantially to the pervasive and profound cognitive deficits observed in patients with this illness. Developments in functional imaging have facilitated the investigation of the neural basis of these cognitive deficits. A strong tradition within neuropsychology has been that circumscribed lesions provide observations which constrain theoretical models, and generate testable predictions on the basis of observed relationships between structural abnormalities and behavioural dysfunction. In this article, the extent to which the neuropsychological tradition can be applied to neuropsychiatry to advance understanding of the biological basis of working memory is addressed. Empirical studies in schizophrenia research are reviewed in relation to principles of normal brain function sub-serving working memory: the functional role of the lateral prefrontal cortex, physiological response capacity constraints, inter-regional functional integration, and compensatory adaptations. However, complex heterogeneous psychiatric disorders such as schizophrenia cannot be considered akin to a pure lesion model, and there are considerable methodological challenges in interpreting disruptions of working memory in psychiatric conditions, resulting from clinical, treatment and performance related confounds. The increasing use of psychopharmacological models of disease in healthy human subjects is therefore considered as an attempt to address, or to some extent circumvent these issues.
What Can Research on Schizophrenia Tell Us about the Cognitive Neuroscience of Working Memory?
Deanna M. Barch
Work with individuals with lesions to specific brain regions has long been used to test or even generate theories regarding the neural systems that support specific cognitive processes. Work with individuals who have neuropsychiatric disorders that also involve neurobiological disturbances may be able to play a similar role in theory testing and building. For example, schizophrenia is a psychiatric disorder thought to involve a range of neurobiological disturbances. Further, individuals with schizophrenia are known to suffer from deficits in working memory, meaning that examining the work on the neurobiology of working memory deficits in schizophrenia may help to further our understanding of the cognitive neuroscience of working memory. This article discusses the pros and cons of extrapolating from work in schizophrenia to models of healthy working memory function, and reviews the literature on working memory function in schizophrenia in relationship to existing human and non-human primate models of the cognitive neuroscience of working memory.
Interfering with working memory in humans
Felix M. Mottaghy
The interference method transcranial magnetic stimulation (TMS) has to be seen as a complimentary tool to the other noninvasive correlational techniques such as positron emission tomography (PET), functional magnetic resonance imaging (fMRI) or electroencephalography (EEG) in cognitive neuroscience. However, the combination of two methods e.g. TMS and PET seems to be the strongest approach to validate or postulate new hypotheses. In this review several studies using TMS to disentangle working memory functions are presented. The conclusion is drawn that there exists a superordinated amodal central executive within the dorsolateral prefrontal cortex strongly connected with modality specific areas mainly within the prefrontal cortex.
Assessing the working memory network: Studies with fMRI and structural equation modeling
Ralf G. M. Schlëśsser, Gerd Wagner, Heinrich Sauer
A considerable body of evidence supports the notion that the neurofunctional mb_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 towards 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.
Part II: What does research in cognitive neuroscience tell us about working memory?
The aim of the second part is to provide more specific reviews of individual research problems within the area of working memory and methods of tackling them. Each paper brings up an individual research question and presents the possible answers that cognitive neuroscience offers today. Papers in the second part typically outline a research problem, present its theoretical background and an overview of empirical research that might point to a specific answer. They provide an insight in and an overview of contemporary research projects in the field of working memory.
Banishing the Homunculus: Making Working Memory Work
Thomas E. Hazy, Michael J. Frank, Randall C. O'Reilly
The prefrontal cortex (PFC) has long been thought to subserve both working memory and âexecutiveâ function, but the mechanistic basis of their integrated function has remained poorly understood, often amounting to a homunculus. This paper reviews the progress in our lab and others pursuing a long-term research agenda to deconstruct this homunculus by elucidating the precise computational and neural mechanisms underlying these phenomena. We outline six key functional demands underlying work- ing memory, and then describe the current state of our computational model of the PFC and associated systems in the basal ganglia (BG). The model, called PBWM (prefrontal-cortex, basal-ganglia working memory model), relies on actively maintained representations in the PFC, which are dynamically up- dated/gated by the BG. It is capable of developing human-like performance largely on its own by taking advantage of powerful reinforcement learning mechanisms, based on the midbrain dopaminergic system and its activation via the BG and amygdala. These learning mechanisms enable the model to learn to control both itself and other brain areas in a strategic, task-appropriate manner. The model can learn challenging working memory tasks, and has been corroborated by several important empirical studies.
Beyond bistability: Biophysics and temporal dynamics of working memory
Daniel Durstewitz, Jeremy K. Seamans
Working memory has often been modeled and conceptualized as a kind of binary (bistable) memory switch, where stimuli turn on plateau-like persistent activity in subsets of cells, in line with many in vivo electrophysiological reports. A potentially related form of bistability, termed up- and down-states, has been studied with regards to its synaptic and ionic basis in vivo and in reduced cortical preparations. Also single cell mechanisms for producing bistability have been proposed and investigated in brain slices and computationally. Recently, however, it has been emphasized that clear plateau-like bistable activity is rather rare during working memory tasks, and that neurons exhibit a multitude of different temporally unfolding activity profiles and temporal structure within their spiking dynamics. Hence, working memory seems to be a highly dynamical neural process with yet unknown mappings from dynamical to computational properties. Empirical findings on ramping activity profiles and temporal structure will be reviewed, as well as neural models that attempt to account for it and its computational significance. Furthermore, recent in vivo, neural culture, and in vitro preparations will be discussed that offer new possibilities for studying the biophysical mechanisms underlying computational processes during working memory. These preparations have revealed additional evidence for temporal structure and spatio-temporally organized attractor states in cortical networks, as well as for specific computational properties that may characterize synaptic processing during high-activity states as during working memory. Together such findings may lay the foundations for highly dynamical theories of working memory based on biophysical principles.
Computational and in vitro studies of persistent activity: Edging towards cellular and synaptic mechanisms of working memory
Albert Compte
Persistent neural activity selective to features of an extinct stimulus has been identifed as the neural correlate of working memory processes. The precise nature of the physiological mb_substrate for this self-sustained activity is still unknown. In the last few years, this problem has gathered experimental together with computational neuroscientists in a quest to identify the cellular and network mechanisms involved. I introduce here the attractor theory framework within which current persistent activity computational models are built, and I then review the main physiological mechanisms that have been linked thereby to persistent activity and working memory. Open computational and physiological issues with these models are discussed, together with their potential experimental validation in current in vitro models of persistent activity.
Dopaminergic control of working memory and its relevance to schizophrenia: a circuit dynamics perspective
Shoji Tanaka
This article argues how dopamine (DA) controls working memory and how the dysregulation of the dopaminergic system is related to schizophrenia. In the dorsolateral prefrontal cortex (DLPFC), which is the principal part of the working memory system, recurrent excitation is subtly balanced with intracortical inhibition. A potent controller of the DLPFC circuit is the mesocortical dopaminergic system. To understand the characteristics of the dopaminergic control of working memory, the stability of the circuit dynamics under the influence of DA has been studied. Recent computational studies suggest that the hyperdopaminergic state is usually stable but the hypodopaminergic state tends to be unstable. The stability also depends on the efficacy of the glutamatergic transmission in the corticomesencephalic projections to DA neurons. When this cortical feedback is hypoglutamatergic, the circuit of the DLPFC tends to be unstable, such that a slight increase in DA releasability causes a catastrophic jump of the DLPFC activity from a low to a high level. This may account for the seemingly paradoxical overactivation of the DLPFC observed in schizophrenic patients. Given that DA transmission is abnormal in the brains of patients with schizophrenia and working memory deficit is a core dysfunction in schizophrenia, the concept of circuit stability would be useful not only for understanding the mechanisms of working memory processing but for developing therapeutic strategies to enhance cognitive functions in schizophrenia.
Prefrontal and parietal contributions to spatial working memory
Clayton E. Curtis
Functional neuroimaging studies consistently implicate a widespread network of human cortical brain areas that together support spatial working memory. This review summarizes our recent functional magnetic resonance imaging (fMRI) studies of humans performing delayed-saccades. These studies have isolated persistent activity in dorsal prefrontal regions, like the frontal eye fields (FEF), and the posterior parietal cortex (PPC) during the maintenance of positional information. We aim to gain insight into the type of information coded by this activity. By manipulating the sensory and motor demands of the working memory task, we have been able to modulate the FEF and PPC delay-period activity. These findings are discussed in the context of other neurophysiological and lesion-based data and some hypotheses regarding the differential contributions of frontal and parietal areas to spatial working memory are offered. Namely, retrospective sensory coding of space may be more prominent in the PPC, while prospective motor coding of space may be more prominent in the FEF.
Brain Mechanisms of Proactive Interference in Working Memory
John Jonides, Derek Evan Nee
It has long been known that storage of information in working memory suffers as a function of proactive interference. Here we review the results of experiments using approaches from cognitive neuroscience to reveal a pattern of brain activity that is a signature of proactive interference. Many of these results derive from a single paradigm that requires one to resolve interference from a previous experimental trial. The importance of activation in left inferior frontal cortex is shown repeatedly using this and other tasks. We review a number of models that might account for the behavioral and imaging findings about proactive interference, raising questions about the adequacy of these models.
Working memory for order information: Multiple cognitive and neural mechanisms.
Christy Marshuetz, Edward E. Smith
Working memory for order information is mediated by differed cognitive mechanisms that rely on different neural circuits. Here we discuss evidence that order memory involves mechanisms that range from general supervisory processes to process that maintenance fine-grained temporal position information. We suggest that neural regions -- including the prefrontal cotex, motor cortex, parietal cortex and medial temporal structures -- operate at different levels and processing stages to give rise to working memory for order information.
Interactions between attention and working memory
Edward Awh, Edward K. Vogel, Sei-Hwan Oh
Studies of attention and working memory address the fundamental limits in our ability to encode and maintain behaviorally relevant information, processes that are critical for goal-driven processing. Here we review our current understanding of the interactions between these processes, with a focus on how each construct encompasses a variety of dissociable phenomena. Attention facilitates target processing during both perceptual and postperceptual stages of processing, and functionally dissociated processes have been implicated in the maintenance of different kinds of information in working memory. Thus, although it is clear that these processes are closely intertwined, the nature of these interactions depends upon the specific variety of attention or working memory that is considered.
Exploration of the neural mb_substrates of executive functioning by functional neuroimaging
Fabienne Collette, Michaël Hogge, Eric Salmon, Martial Van der Linden
This review presents neuroimaging studies that have explored the cerebral mb_substrates of executive functioning. These studies have demonstrated that different executive functions not only recruit various frontal areas but also depend upon posterior (mainly parietal) regions. These results are in accordance with the hypothesis that executive functioning relies on a distributed cerebral network that is not restricted to anterior cerebral areas. However, there exists an important heterogeneity in the cerebral areas associated with these different processes, and also between different tasks assessing the same process. Since these discrepant results could be due to the paradigms used (subtraction designs), recent results obtained with conjunction and interaction analyses are presented, which confirm the role of parietal areas in executive functioning and also demonstrate the existence of some specificity in the neural mb_substrates of the executive processes of updating, shifting and inhibition. Finally, fMRI studies show that the activity in cerebral areas involved in executive tasks can be transient or sustained. Consequently, to better characterise the functional role of areas associated with executive functioning, it is important to take into account not only the localisation of cerebral activity but also the temporal pattern of this activity.
Factors Controlling Neural Activity during Delayed-response Task Performance: Testing a Memory Organization Hypothesis of Prefrontal Function
Bart Rypma
Understanding the role of prefrontal cortex (PFC) in delayed-response task performance has been a central focus of neuroimaging research. The first part of this review will emphasize consistent observations of memory-load-related effects on PFC activity that has led me and my colleagues to propose a âmemory-organization hypothesisâ of PFC function. The second part examines how predictions of this hypothesis have borne up to empirical testing. The final part of this review suggests that there is important information contained in between-study variance in the anatomical locus and temporal sequence of neural activity. I will examine how subtle variations in task-structure affect subjects' strategies, producing meaningful variability in neuroimaging data. Systematic manipulation of these variables in future research can assist in elucidating the role of PFC in delayed response task performance.
Maintenance of Multiple Working Memory Items by Temporal Segmentation
Ole Jensen
Experimental work based on single cell recordings support the hypothesis that work- ing memory representations are retained by sustained neuronal firing. While this hypothesis can account for the maintenance of a single memory item, it remains un- clear how multiple working memory items are represented. This account will discuss the possible physiological mechanism responsible for the maintenance of multiple working memory items including mechanisms based on sustained firing and synaptic encoding. The focus will be on temporal segmentation by phase encoding, namely the idea that several working memory items are activated sequentially at different points in time. It has been proposed that a mechanism of nested gamma (30-80 Hz) and theta (4â8 Hz) oscillations is responsible for controlling the reactivation of the memory list. This mechanism has been shown to be compatible with mul- tiple behavioral findings on working memory such as the data from the Sternberg experiment. The theta/gamma mechanism has also received support from a large set of electrophysiological findings, however, more experimental work is required to further substantiate or falsify the model.
Prefrontal cortex and working memory processes
Shintaro Funahashi
Working memory is a mechanism for short-term active maintenance of information as well as for processing maintained information. The dorsolateral prefrontal cortex (DLPFC) has been known to participate in working memory. The analysis of task- related DLPFC activity while monkeys performed a variety of working memory tasks revealed that delay-period activity is a neural correlate of a mechanism for temporary active maintenance of information, because this activity persisted throughout the delay period, showed selectivity to a particular visual feature, and was related to correct behavioral performances. Information processing can be considered as a change of the information represented by a population of neural activities during the progress of the trial. Using population vectors calculated by a population of task-related DLPFC activities, we demonstrated the temporal change of information represented by a population of DLPFC activities during performances of spatial working memory tasks. Cross-correlation analysis using spike firings of simultaneously isolated pairs of neurons reveals widespread functional interactions among neighboring neurons, especially neurons having delay-period activity, and their dynamic modulation depending on the context of the trial. Functional interactions among neurons and their dynamic modulation could be a mechanism of information processing in the DLPFC.
Under the Curve: Critical Issues for Elucidating D1 Receptor Function in Working Memory
Graham V. Williamsa, Stacy A. Castner
It has been postulated that spatial working memory operates optimally within a limited range of dopamine transmission and D1 receptor signaling in prefrontal cortex. Insufficiency in prefrontal dopamine, as in aging, and excessive transmission, as in acute stress, lead to impairments in working memory that can be ameliorated by D1 receptor agonist and antagonist treatment, respectively. Iontophoretic investigations of dopamine's influence on the cellular mechanisms of working memory have revealed that moderate D1 blockade can enhance memory fields in primate prefrontal pyramidal neurons while strong blockade abolishes them. The combined behavioral and physiological evidence indicates that there is a normal range of dopamine function in prefrontal cortex that can be described as an âinverted-Uâ relationship between dopamine transmission and the integrity of working memory. Both in vivo and in vitro studies have demonstrated a role for dopamine in promoting the excitability of prefrontal pyramidal cells and facilitating their NMDA inputs, while simultaneously restraining recurrent excitation and facilitating feedforward inhibition. This evidence indicates that there is a fine balance between the synergistic mechanisms of D1 modulation in working memory. Given the critical role of prefrontal function for cognition, it is not surprising that this balancing act is perturbed by both subtle genetic influences and environmental events. Further, there is evidence for an imbalance in these dopaminergic mechanisms in multiple neuropsychiatric disorders, particularly schizophrenia, and in related nonhuman primate models. Elucidating the orchestration of dopamine signaling in key nodes within prefrontal microcircuitry is therefore pivotal for understanding the influence of dopamine transmission on the dynamics of working memory. Here, we explore the hypothesis that the window of optimal dopamine signaling changes on a behavioral time-scale, dependent upon current cognitive demands and local neuronal activity as well as long-term alterations in signaling pathways and gene expression. If we look under the bell-shaped curve of prefrontal dopamine function, it is the relationship between neuromodulation and cognitive function that promises to bridge our knowledge between molecule and mind.
Working memory for visual objects: Complementary roles of inferior temporal, medial temporal, and prefrontal cortex
Charan Ranganath
Humans have an extraordinary ability to maintain and manipulate visual image information in the absence of perceptual stimulation. The neural mb_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.
Part III: Recent findings on working memory
The goal of the third part is to present state of the art empirical papers from the field of working memory that are examples of how individual research questions can be dealt with in empirical research. The aim of this part is on one side to show the variability of the current research questions and on the other the state of the current methods and techniques in the fields of cognitive neuroscience.
Successful declarative memory formation is associated with ongoing activity during encoding in a distributed neocortical network related to working memory: An MEG study
Atsuko Takashima, Ole Jensen, Robert Oostenveld, Eric Maris, Mara van de Coevering, Guillen Fernandez
The aim of the present study was to investigate the spatio-temporal characteristics of the neural correlates of declarative memory formation as assessed by the subsequent memory effect, i.e. the difference in encoding activity between subsequently remembered and subsequently forgotten items. Different operations could account for these effects. In particular, it has been proposed that successful memory formation depends on the organization of the information at the time of encoding, an operation accomplished by the working memory system. Consequently, functional magnetic resonance imaging (fMRI) studies have already shown that the very same regions that are involved in certain working memory processes are also involved in declarative memory formation. Here, we used magnetoencephalography (MEG) to investigate whether the subsequent memory effects in these regions are present throughout picture stimulus presentation, postulating ongoing working memory operations as an effective factor. The results showed that subsequent memory effects began to appear after about 300 ms post stimulus onset over bilateral temporal areas and left parietal regions and were sustained throughout the recording epoch (1000 ms). Roughly parallel to these effects, we identified a left frontal subsequent memory effect, which, however, was less sustained than the other effects. In addition, we revealed a late subsequent memory effect over the right occipital region, which has not been described previously in the event-related potential (ERP) literature. These sustained subsequent memory effects are suggestive of working memory processes that may enable deep semantic and perceptual processing. Additionally, contextually constrained visual perception after top- down modulation may account for a more efficient encoding of the complex scene.
Sequential neural processes of tactile-visual crossmodal working memory
Shinji Ohara, Fred A Lenz, Yongdi Zhou
Working memory is essential to learning and performing sensory-motor behaviors that in many situations require the integration of stimuli of one modality with stimuli of another. In the present study, we focused on the neural mechanisms underlying crossmodal working memory. We hypothesized that in performance of the tactile crossmodal working memory task, there would be sequentially discrete task-correlated neural activities representing the processes of crossmodal working memory.
Scalp-recorded event-related potentials (ERPs) were collected from 15 electrodes in humans performing each of four tasks: tactile-tactile unimodal delayed matching-to-sample task, tactile-visual crossmodal delayed matching-to- sample task, tactile unimodal control spatial task, and tactile crossmodal control spatial task. Two positive ERP peaks were observed during the delay of the task. One peak (LPC-1, late positive component-1) was at about 330 ms after the onset of the tactile stimulus, and the other (LPC-2, late positive component-2) was at about 600 ms. LPC-1 was observed in all four tasks. There was no significant difference in LPC-1 either between the unimodal tasks, or between the crossmodal tasks, but LPC-1 was significantly larger in the crossmodal tasks than that in the unimodal tasks, and showed a specific pattern of larger activity over parietal areas than activity over frontal areas. LPC-2 was not observed in the unimodal matching task but was observed in all other three tasks over parietal areas. During the late delay (1,000 ms -1,500 ms), significant differences in negative potentials (late negative component, LNC) was found between the tasks.
The present study shows sequential changes in ERPs during the retention period of working memory tasks. It indicates that in performance of a crossmodal working memory task, there are sequentially discrete neural processes that may represent neural activities related to different cognitive functions, such as crossmodal transfer of information, and the working memory of the stimulus.
Working memory for order and the parietal cortex: an event-related fMRI study
Christy Marshuetz, Patricia A. Reuter-Lorenz, Edward E. Smith, John Jonides, Douglas C. Noll
Memory for order information has been tied to the frontal lobes, however, parietal activation is observed in many functional neuroimaging studies. Here we report functional magnetic resonance findings from an event-related experiment involving working memory for order. Five letters were presented for storage, followed after a delay by two probe items. Probe items could be separated by 0-3 positions in the memory set and subjects had to indicate whether the items were in the correct order. Analyses indicate that activation in left parietal cortex shows a systematic decrease in activation with increasing probe distance. This finding is consistent with an earlier study in which we suggested that parietal cortical regions mediate the representation of order information via magnitude codes.
Functional Connectivity Reveals Load Dependent Neural Systems Underlying Encoding and Maintenance in Verbal Working Memory
Todd S. Woodward, Tara A. Cairo, Christian C Ruff, Yoshio Takane, Michael A Hunter, Elton T. C. Ngan
One of the main challenges in working memory research has been to understand the degree of separation and overlap between the neural systems involved in encoding and maintenance. In the current study we used a variable load version of the Sternberg item recognition test (SIRT; 2, 4, 6, or 8 letters) and a functional connectivity method based on constrained principal component analysis (CPCA) to extract load-dependent neural systems underlying encoding and maintenance, and to characterize their anatomical overlap and functional interaction. Based on the pattern of functional connectivity, CPCA identified a load-dependent encoding system comprising bilateral occipital (BA 17, 18), bilateral superior parietal (BA 7), bilateral dorsolateral prefrontal (BA 46), and dorsal anterior cingulate (BA 24, 32) regions. For maintenance, in contrast, CPCA identified a system that was characterized by both load- dependent increases and decreases in activation. The structures in this system jointly activated by maintenance load involved left posterior parietal (BA 40), left inferior prefrontal (BA 44), left premotor and supplementary motor areas (BA 6), and dorsal cingulate regions (BA 24, 32), while the regions displaying maintenance-load-dependent activity decreases involved bilateral occipital (BA 17, 18), posterior cingulate (BA 23) and rostral anterior cingulate/orbitofrontal (BA 10, 11, 32) regions. The correlation between the encoding and maintenance systems was strong and negative (Pearson's r = -.55), indicting that some regions important for visual processing during encoding displayed reduced activity during maintenance, while subvocal rehearsal and phonological storage regions important for maintenance showed a reduction in activity during encoding. In summary, our analyses suggest that separable and complementary subsystems underlie encoding and maintenance in verbal working memory, and they demonstrate how CPCA can be employed to characterize neuronal systems and their functional contributions to higher-level cognition.
The functional neuroanatomy of classic delayed response tasks in humans and the limitations of cross-method convergence in prefrontal function
Gary R. Turner, Brian Levine
Three classic delay tasks: spatial delayed response, delayed spatial alternation and delayed object-alternation are prototypical experimental paradigms for mapping the functional neuroanatomy of prefrontal cortex in animals. These tasks have been applied in human lesion studies, yet there have been very few studies investigating their functional neuroanatomy in healthy human subjects. We used fMRI to investigate the functional neuroanatomy of these classic paradigms (and a fourth: object delayed response) in a single sample of healthy human participants. Consistent with previous animal, human lesion, and functional neuroimaging studies, activity was observed in prefrontal and posterior parietal cortices across all three delay tasks. Task-specific activations, however, were not entirely consistent with predictions drawn from animal lesion studies. For example, delayed object-alternation activated dorsolateral PFC, a region not generally implicated in animal lesion reports. Spatial delayed response, classically associated with the dorsolateral PFC, did not activate this region; it rather activated posterior premotor cortices involved in response preparation, as did spatial alternation. All three tasks activated the frontopolar cortex, a region not considered crucial in animal research but associated with manipulation of internally generated information in recent human research. While cross method convergence may be attained for lower level perceptual or motor tasks, the results of this study caution against the assumption that lesion-specific effects in animals generalize to human PFC function.
Neural correlates of spatial working memory in humans: A fmri study comparing visual and tactile processes
Emiliano Ricciardi, Daniela Bonino, Claudio Gentili, Lorenzo Sani, Pietro Pietrini, Tomaso Vecchi
Recent studies of neural correlates of working memory components have identified both low-level perceptual processes and higher-order supramodal mechanisms through which sensory information can be integrated and manipulated. In addition to the primary sensory cortices, working memory relies on a widely distributed neural system of higher-order association areas that includes posterior parietal and occipital areas, and on prefrontal cortex (PFC) for maintaining and manipulating information. The present study was designed to determine brain patterns of neural response to the same spatial working memory task presented either visually or in a tactile format, and to evaluate the relationship between spatial processing in the visual and tactile sensory modalities. Brain activity during visual and tactile spatial working memory tasks was measured in six young right-handed healthy male volunteers by using functional magnetic resonance imaging (fMRI). Results indicated that similar fronto- parietal networks were recruited during spatial information processing across the two sensory modalities â specifically the posterior parietal cortex, the dorsolateral PFC and the anterior cingulate cortex. These findings provide a neurobiological support to behavioral observations by indicating that common cerebral regions subserve generation of higher order mental representations involved in working memory independently from a specific sensory modality.
Neural mb_substrates of manipulation in visuospatial working memory
Boris Suchan, Robin Botko, Elke Gizewski, Michael Forsting, Irene Daum
The present study aimed to investigate whether similar neuronal mechanisms underlie the manipulation and active processing of visual and visuospatial stimuli. Simultaneous and successive mental rotation and identity judgment of 2-D matrices and 3-D cube figures were contrasted using fMRI. Results demonstrate that activation patterns during mental rotation with low working memory demands differ depending on stimulus type (2-D vs. 3-D). Comparison of simultaneous mental rotation of matrices and 3-D cubes resulted in activation of frontal as well as inferior and superior parietal cortices. The opposite contrast (mental rotation of 3- D cubes vs. 2-D matrices) yielded only frontal cortex activation. The findings also yield evidence for converging, overlapping activation pattern for 2-D and 3-D stimuli if working memory demands are increased. Results are discussed within the frame-work of current working memory models.
A functional MRI study of the effects of pergolide, a dopamine receptor agonist, on component processes of working memory
Sasha E.B. Gibbs, Mark D'Esposito
Working memory is an important cognitive process dependent on a network of prefrontal and posterior cortical regions. In this study we tested the effects of the mixed D1-D2 dopamine receptor agonist pergolide on component processes of working memory using functional magnetic resonance imaging (fMRI). An event-related trial design allowed separation of the effects on encoding, maintenance, and retrieval processes. Subjects were tested with spatial and object memoranda to investigate modality-specific effects of dopaminergic stimulation. We also measured baseline working memory capacity as previous studies have shown that effects of dopamine agonists vary with working memory span. Pergolide improved reaction time for high-span subjects and impaired reaction time for low-span subjects. This span-dependent change in behavior was accompanied by span-dependent changes in delay-related activity in the premotor cortex. We also found evidence for modality-specific effects of pergolide only during the response period. Pergolide increased activity for spatial memoranda and decreased activity for object memoranda in task-related regions including the prefrontal and parietal cortices.
Socioaffective factors modulate working memory in schizophrenia patients.
Sohee Park, Crystal Gibson, Tara McMichael
Working memory (WM) deficit in schizophrenia is a core cognitive feature of the disorder and is reliably associated with abnormalities of the prefrontal circuitry. WM deficits are also associated with impaired social functioning and present a major obstacle towards successful rehabilitation in schizophrenia. Although the role of prefrontal cortex (PFC) in WM has been extensively investigated, the intricate relations among the prefrontal circuitry, WM and social behaviors are not clearly understood. In this study, we manipulated social context and observed their effects on spatial WM. In Experiment 1, the effects of social and asocial reinforcements on spatial WM were examined in schizophrenic patients and healthy controls. The results show that social but not asocial reinforcements facilitated spatial WM in schizophrenic patients. In Experiment 2, the effects human voice reinforcements (with or without affect) on WM was investigated. Voice reinforcements did not facilitate WM relative to the no-reinforcement condition. There was no difference between high-affect vs flat-affect voice conditions. In Experiment 3, the effects of direct and indirect social interactions on spatial WM were studied. Direct but not indirect social interaction facilitated WM in schizophrenic patients. These results suggest that social context might facilitate WM in schizophrenic patients perhaps by activating frontal lobe systems. In addition, the possibility of improving cognitive functions such as WM using seemingly non-cognitive methods might lead to potential remediation strategies.
The use of working memory for task prediction: what benefits accrue from different types of foreknowledge?
Jason Barton, Aaron Kuzin, Frida E. Polli, Dara S. Manoach
The assumption that the deployment of executive processes invariably improves task performance is implicit to cognitive theory. In particular, working memory can be used to retain and update historical information about predictable trial sequences (foreknowledge) so that subjects can anticipate and prepare for the upcoming trial more effectively. We review the effects of different types of foreknowledge on response accuracy and latency, particularly in relation to experiments investigating saccadic eye movements. While it is possible to make all aspects of an impending trial predictable, varying the predictability of different components of the trial independently can reveal which cognitive operations are potentially modifiable by foreknowledge. These operations include stimulus processing, retrieval of task-set rules, and response preparation, among others. The available data suggest that, while response preparation can be completed and the response even executed before the stimulus appears (i.e. anticipation) when the subject possesses complete task-foreknowledge (knowing both the stimulus to appear and the response required), foreknowledge of the task-set alone does not permit advance configuration of the task-set rules. A taxonomy for foreknowledge is proposed, including foreknowledge for timing, stimulus, set, response, and task. Work on differentiating these effects in neurophysiology, neuroimaging, and neuropsychology is still in the early stages.
Symmetry and binding in visuo-spatial working memory
Clelia Rossi-Arnaud, Laura Pieroni, Alan Baddeley
Three experiments study the impact of symmetry on a sequential block tapping immediate memory task. Experiment 1 shows an advantage from vertical symmetry over non symmetrical sequences, while finding no effect of horizontal or diagonal symmetry. Experiment 2 tests the possible role of verbal labelling by means of a secondary task that prevents this by articulatory suppression. No evidence of verbalization was observed. A third study examined the effects of a concurrent executive load, finding an overall impairment, that did not differ between symmetrical and asymmetric patterns, suggesting that the effect of symmetry reflects automatic rather than executive processes. Implications for the episodic buffer component of working memory are discussed.
Working memory and acquisition of implicit knowledge by imagery training, without actual task performance
Andre Frazeo Helene, Gilberto Fernando Xavier
This study investigated acquisition of a mirror-reading skill via imagery training, without the actual performance of a mirror-reading task. In Experiment I, healthy volunteers simulated writing on an imaginary, transparent screen placed at eye level, which could be read by an experimenter facing the subject. Performance of this irrelevant motor task required the subject to imagine the letters inverted, as if seen in a mirror from their own point of view (imagery training). A second group performed the same imagery training interspersed with a complex, secondary spelling and counting task. A third, control, group simply wrote the words as they would normally appear from their own point of view. After training with 300 words, all subjects were tested in a mirror-reading task using 60 non-words, constructed according to acceptable letter combinations of the Portuguese language. Compared to control subjects, those exposed to imagery training, including those who switched between imagery and the complex task, exhibited shorter reading times in the mirror-reading task. Experiment II employed a 2 x 3 design, including two training conditions (imagery and actual mirror-reading) and three competing task conditions (a spelling and counting switching task, a visual working memory concurrent task, and no concurrent task). Training sessions were interspersed with mirror-reading testing sessions for non-words, allowing evaluation of the mirror-reading acquisition process during training. The subjects exposed to imagery training acquired the mirror- reading skill as quickly as those exposed to the actual mirror-reading task. Further, performance of concurrent tasks together with actual mirror-reading training severely disrupted mirror-reading skill acquisition; this interference effect was not seen in subjects exposed to imagery training and performance of the switching and the concurrent tasks. These results unequivocally show that acquisition of implicit skills by top-down imagery training is at least as efficient as bottom-up acquisition.
