Binding in visual working memory: the role of the episodic buffer

The episodic buffer component of working memory is assumed to play a central role in the binding of features into objects, a process that was initially assumed to depend upon executive resources. Here, we review a program of work in which we specifically tested this assumption by studying the effects of a range of attentionally demanding concurrent tasks on the capacity to encode and retain both individual features and bound objects. We found no differential effect of concurrent load, even when the process of binding was made more demanding by separating the shape and color features spatially, temporally or across visual and auditory modalities. Bound features were however more readily disrupted by subsequent stimuli, a process we studied using a suffix paradigm. This suggested a need to assume a feature-based attentional filter followed by an object based storage process. Our results are interpreted within a modified version of the multicomponent working memory model. We also discuss work examining the role of the hippocampus in visual feature binding.     

Right-sided representational neglect after left brain damage in a case without visuospatial working memory deficits

Brain damaged patients suffering from representational neglect (RN) fail to report, orient to, or verbally describe contra-lesional elements of imagined environments or objects. So far this disorder has only been reported after right brain damage, leading to the idea that only the right hemisphere is involved in this deficit. A widely accepted account attributes RN to a lateralized impairment in the visuospatial component of working memory. So far, however, this hypothesis has not been tested in detail. In the present paper, we describe, for the first time, the case of a left brain damaged patient suffering from right-sided RN while imagining both known and new environments and objects. An in-depth evaluation of her visuospatial working memory abilities, with special focus on the presence of a lateralized deficit, did not reveal any abnormality. In sharp contrast, her ability to memorize visual information was severely compromised. The implications of these results are discussed in the light of recent insights in the neglect syndrome.     

Direction specific costs to spatial working memory from saccadic and spatial remapping

Right parietal lesions often lead to neglect, in which patients fail to attend to leftward stimuli. Recent models of neglect suggest that, in addition to attentional impairments, patients demonstrate impairments of spatial remapping and/or spatial working memory (SWM). Although spatial remapping could be considered a kind of spatial memory process itself (i.e., updating remembered locations based on anticipated saccade outcomes), the two processes operate on very different time scales (milliseconds versus seconds). In the present study, we examined the influence of saccadic and covert spatial remapping on SWM in healthy individuals. An initial control condition in which subjects had to respond to a probe stimulus (i.e., is the probe in the location previously occupied by the target?) following a 1500ms delay was contrasted with conditions in which the fixation point moved (left, right, up, or down) at the onset of the delay. In a second version of the task, participants made covert shifts of attention at delay onset requiring covert spatial, rather than saccadic, remapping. In both tasks SWM performance was best when no remapping was required with the largest decrements in SWM being observed in the covert spatial remapping task. For both saccadic and covert spatial remapping, a consistent cost was observed for remapping the target array into right visual space. Results are discussed in terms of hemispheric biases in attention and differences in performance for peripersonal versus extrapersonal space.     

A comparative study of working memory: immediate serial spatial recall in baboons (Papio papio) and humans

Two experiments assessed if non-human primates can be meaningfully compared to humans in a non-verbal test of serial recall. A procedure was used that was derived from variations of the Corsi test, designed to test the effects of sequence structure and movement path length in humans. Two baboons were tested in Experiment 1. The monkeys showed several attributes of human serial recall. These included an easier recall of sequences with a shorter number of items and of sequences characterized by a shorter path length when the number of items was kept constant. However, the accuracy and speed of processing did not indicate that the monkeys were able to benefit from the spatiotemporal structure of sequences. Humans tested in Experiment 2 showed a quantitatively longer memory span, and, in contrast with monkeys, benefitted from sequence structure. The results are discussed in relation to differences in how human and non-human primates segment complex visual patterns.     

Prose recall and amnesia: implications for the structure of working memory

Two densely amnesic patients are shown to have good immediate but poor delayed prose recall, a result that presents problems for the current multi-component model of working memory. Examination of a wide sample of memory impaired patients suggests that this pattern occurs in densely amnesic patients who have well-preserved intelligence and good executive capacities. Patients suffering from Alzheimer's disease typically show poor immediate and delayed prose recall, reflecting their combined intellectual and memory deficits. The results are interpreted in terms of a proposed new component of working memory, the episodic buffer.     

Disentangling working memory processes during spatial span assessment: A modeling analysis of preferred eye movement strategies

The neurocognitive processes involved during classic spatial working memory (SWM) assessment were investigated by examining naturally preferred eye movement strategies. Cognitively healthy adult volunteers were tested in a computerized version of the Corsi Block-Tapping Task—a spatial span task requiring the short term maintenance of a series of locations presented in a specific order—coupled with eye tracking. Modeling analysis was developed to characterize eye-tracking patterns across all task phases, including encoding, retention, and recall. Results revealed a natural preference for local gaze maintenance during both encoding and retention, with fewer than 40% fixated targets. These findings contrasted with the stimulus retracing pattern expected during recall as a result of task demands, with 80% fixated targets. Along with participants’ self-reported strategies of mentally “making shapes,” these results suggest the involvement of covert attention shifts and higher order cognitive Gestalt processes during spatial span tasks, challenging instrument validity as a single measure of SWM storage capacity.     

Visual spatial and visual pattern working memory: neuropsychological evidence for a differential role of left and right dorsal visual brain

According to neurophysiological, neuroimaging, and behavioural evidence, visual working memory (WM) can be separated into a "what" and a "where" component, reflecting the duality of visual processing. Whereas a wealth of empirical data suggests a right-sided fronto-parietal network critical for the maintenance of spatial information, the cortical structures underlying maintenance of object information have remained controversial. Although visual object processing depends on ventral, inferior temporal areas, recent neuroimaging results suggest that maintenance of visual object information involves a left-sided or bilateral fronto-parietal network. The aim of the present study is to further clarify the role of the left and right parietal lobes for pattern and spatial visual WM. Seven patients with left-sided, seven with right-sided parietal brain injury, and two age-matched healthy control groups performed a delayed-matching-to-sample task using either pattern (shape) or spatial (location) information or both. In addition, eight patients with left-sided injury sparing parietal areas were tested to further examine the specific role of the left parietal cortex in pattern WM. Left parietal injury resulted in pattern WM impairment, only, while right parietal injury was associated with pattern and spatial WM deficits. Non-parietal injury was not associated with comparable deficits. These results suggest that visual spatial WM depends critically on right parietal areas; in contrast, pattern WM depends on both, left and right parietal areas.     

Biasing visual selection: functional neuroimaging of the interplay between spatial cueing and feature memory guidance

The authors investigate the interplay between spatial attention and memory-based feature guidance of visual selection. Three types of guidance were tested: working memory, spatial cueing and passive memory. In all cases the memory-cue was not relevant to a subsequent search task, whilst the spatial cue always provided valid information. Behaviourally, search performance was influenced by spatial cueing and by feature-based cueing from the contents of working memory; both forms of guidance interacted, with feature guidance being more effective when the target's location was not pre-cued. Spatial cueing recruited the dorsal fronto-parietal network which was silent during the WM-only condition. Memory guidance of selection was reflected in activity in a frontal-temporal-occipital network. Interestingly, when spatial and memory guidance were pitted against each other, neural activity in this latter network was greatly attenuated. Connectivity analysis showed that the posterior parietal cortices inhibit the responses of occipital and temporal regions to the onset of memory-items in the search display. In the presence of a reliable spatial cue the posterior parietal cortex resumes control of attentional deployment. These results illustrate how different forms of attention guidance interact to optimise visual selection.     

Verbal and spatial working memory in older individuals: A positron emission tomography study

Recent reviews of a substantial number of studies have partially resolved questions concerning the brain regions used by working memory for manipulation and representation. We report a large single experiment in middle-aged to older adults (n = 89), classified by hypertensive status. Our design addresses the question of regions related to manipulation and representation, most particularly comparing spatial and verbal working memory. A control, memory search, and 2-back running memory task were performed with identical stimuli and responses during whole-brain 15O water positron emission tomography (PET) scans. Letter or spatial position instructions created verbal or spatial working memory versions of the tasks. We assessed agreement with the literature using regions of interest that were defined by clusters of activation empirically derived from the literature by Wager and Smith (Wager, T.D. and Smith, E.E., Neuroimaging studies of working memory: a meta-analysis, Cognitive, Affective and Behavioral Neuroscience, 3 (2003) 255-274). Our results largely confirmed conclusions from the review on the organization of working memory into dorsal prefrontal manipulation and ventrolateral prefrontal maintenance areas and representation in dorsal and ventral paths. Specific verbal versus spatial comparisons were also concordant with prior work establishing posterior lateralized representation for different contents by working memory. The similarity of results between this older sample and results derived by others from younger participants is notable.     

Material-specific long-term memory representations of faces and spatial positions: evidence from slow event-related brain potentials

Motivated by models that propose material-specific cortical long-term memory representations we expected different topographies of event-related slow waves of the EEG during cued retrieval of two distinct types of information (faces and spatial positions), which are assumed to be processed and stored in topographically distinct cortical areas, i.e., in either the ventral or the dorsal visual pathway. Seventeen participants learned associations either between words and spatial positions or between words and faces. Each word was associated with either one or two positions or faces. In a cued recall test, one day later, participants saw two words and had to decide whether these were linked to each other via an associated spatial position or a face. Slow event-related potentials (ERPs) of the EEG were recorded from 61 scalp electrodes during both acquisition and recall. Response times increased monotonically with the number of faces and positions to be reactivated. Negative slow ERPs showed a comparable topography during anticipation learning and cued recall, but dissociated topographically for positions and faces. The maximum of the negativity increased when items were presented repetitively (compared to the first presentation) during learning, and also with the number of the to-be-reactivated associations during retrieval. These results are consistent with an information-processing model that assumes material-specific cortical representations of episodic memory contents, which are established as localized cortical cell assemblies during encoding, and which are being reactivated during recall.     

Translating working memory into action: Behavioral and neural evidence for using motor representations in encoding visuo‐spatial sequences

The neurobiological organization of action‐oriented working memory is not well understood. To elucidate the neural correlates of translating visuo‐spatial stimulus sequences into delayed (memory‐guided) sequential actions, we measured brain activity using functional magnetic resonance imaging while participants encoded sequences of four to seven dots appearing on fingers of a left or right schematic hand. After variable delays, sequences were to be reproduced with the corresponding fingers. Recall became less accurate with longer sequences and was initiated faster after long delays. Across both hands, encoding and recall activated bilateral prefrontal, premotor, superior and inferior parietal regions as well as the basal ganglia, whereas hand‐specific activity was found (albeit to a lesser degree during encoding) in contralateral premotor, sensorimotor, and superior parietal cortex. Activation differences after long versus short delays were restricted to motor‐related regions, indicating that rehearsal during long delays might have facilitated the conversion of the memorandum into concrete motor programs at recall. Furthermore, basal ganglia activity during encoding selectively predicted correct recall. Taken together, the results suggest that to‐be‐reproduced visuo‐spatial sequences are encoded as prospective action representations (motor intentions), possibly in addition to retrospective sensory codes. Overall, our study supports and extends multi‐component models of working memory, highlighting the notion that sensory input can be coded in multiple ways depending on what the memorandum is to be used for. Hum Brain Mapp 35:3465–3484, 2014. © 2013 Wiley Periodicals, Inc .     

Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex

Cognitive behaviour requires complex context-dependent mapping between sensory stimuli and actions. The same stimulus can lead to different behaviours depending on the situation, or the same behaviour may be elicited by different cueing stimuli. Neurons in the primate prefrontal cortex show task-specific firing activity during working memory delay periods. These neurons provide a neural substrate for mapping stimulus and response in a flexible, context- or rule-dependent, fashion. We describe here an integrate-and-fire network model to explain and investigate the different types of working-memory-related neuronal activity observed. The model contains different populations (or pools) of neurons (as found neurophysiologically) in attractor networks which respond in the delay period to the stimulus object, the stimulus position ('sensory pools'), to combinations of the stimulus sensory properties (e.g. the object identity or object location) and the response ('intermediate pools'), and to the response required (left or right) ('premotor pools'). The pools are arranged hierarchically, are linked by associative synaptic connections, and have global inhibition through inhibitory interneurons to implement competition. It is shown that a biasing attentional input to define the current rule applied to the intermediate pools enables the system to select the correct response in what is a biased competition model of attention. The integrate-and-fire model not only produces realistic spiking dynamicals very similar to the neuronal data but also shows how dopamine could weaken and shorten the persistent neuronal activity in the delay period; and allows us to predict more response errors when dopamine is elevated because there is less different activity in the different pools of competing neurons, resulting in more conflict.     

Differences in working memory coding of biological motion attributed to oneself and others

The question how the brain distinguishes between information about self and others is of fundamental interest to both philosophy and neuroscience. In this functional magnetic resonance imaging (fMRI) study, we sought to distinguish the neural substrates of representing a full‐body movement as one''s movement and as someone else''s movement. Participants performed a delayed match‐to‐sample working memory task where a retained full‐body movement (displayed using point‐light walkers) was arbitrarily labeled as one''s own movement or as performed by someone else. By using arbitrary associations we aimed to address a limitation of previous studies, namely that our own movements are more familiar to us than movements of other people. A searchlight multivariate decoding analysis was used to test where information about types of movement and about self‐association was coded. Movement specific activation patterns were found in a network of regions also involved in perceptual processing of movement stimuli, however not in early sensory regions. Information about whether a memorized movement was associated with the self or with another person was found to be coded by activity in the left middle frontal gyrus (MFG), left inferior frontal gyrus (IFG), bilateral supplementary motor area, and (at reduced threshold) in the left temporoparietal junction (TPJ). These areas are frequently reported as involved in action understanding (IFG, MFG) and domain‐general self/other distinction (TPJ). Finally, in univariate analysis we found that selecting a self‐associated movement for retention was related to increased activity in the ventral medial prefrontal cortex.     

Social working memory and its distinctive link to social cognitive ability: an fMRI study

Engaging social working memory (SWM) during effortful social cognition has been associated with neural activation in two neurocognitive systems: the medial frontoparietal system and the lateral frontoparietal system. However, the respective roles played by these systems in SWM remain unknown. Results from this study demonstrate that only the medial frontoparietal system supports the social cognitive demands managed in SWM. In contrast, the lateral frontoparietal system supports the non-social cognitive demands that are needed for task performance, but that are independent of the social cognitive computations. Moreover, parametric increases in the medial frontoparietal system, but not the lateral frontoparietal system, in response to SWM load predicted performance on a challenging measure of perspective-taking. Thus, the medial frontoparietal system may uniquely support social cognitive processes in working memory and the working memory demands afforded by effortful social cognition, such as the need to track another person’s perspective in mind.     

Maternal immune activation targeted to a window of parvalbumin interneuron development improves spatial working memory: Implications for autism

Maternal immune activation (MIA) increases risk for neuropsychiatric disorders such as autism spectrum disorder (ASD) in offspring later in life through unknown causal mechanisms. Growing evidence implicates parvalbumin-containing GABAergic interneurons as a key target in rodent MIA models. We targeted a specific neurodevelopmental window of parvalbumin interneurons in a mouse MIA model to examine effects on spatial working memory, a key domain in ASD that can manifest as either impairments or improvements both clinically and in animal models.Pregnant dams received three consecutive intraperitoneal injections of Polyinosinic:polycytidylic acid (poly(I:C), 5 mg/kg) at gestational days 13, 14 and 15. Spatial working memory was assessed in young adult offspring using touchscreen operant chambers and the Trial-Unique Non-matching to Location (TUNL) task. Anxiety, novelty seeking and short-term memory were assessed using Elevated Plus Maze (EPM) and Y-maze novelty preference tasks. Fluorescent immunohistochemistry was used to assess hippocampal parvalbumin cell density, intensity and co-expression with perineuronal nets. qPCR was used to assess the expression of putatively implicated gene pathways.MIA targeting a window of parvalbumin interneuron development increased spatial working memory performance on the TUNL touchscreen task which was not influenced by anxiety or novelty seeking behaviour. The model reduced fetal mRNA levels of Gad1 and adult hippocampal mRNA levels of Pvalb and the distribution of low intensity parvalbumin interneurons was altered.We speculate a specific timing window for parvalbumin interneuron development underpins the apparently paradoxical improved spatial working memory phenotype found both across several rodent models of autism and clinically in ASD.     

Dissociable dorsal and ventral frontostriatal working memory circuits: Evidence from subthalamic stimulation in Parkinson's disease

In this study, we investigated the neural substrates involved in visual working memory (WM) and the resulting effects of subthalamic nucleus (STN) stimulation in Parkinson's disease (PD). Cerebral activation revealed by positron emission tomography was compared among Parkinson patients with (PD‐ON) or without (PD‐OFF) STN stimulation, and a group of control subjects (CT) in two visual WM tasks with spatial (SP) and nonspatial (NSP) components. PD‐OFF patients displayed significant reaction time (RT) deficits for both memory tasks. Although there were no significant differences in RT between patients with PD‐ON and ‐OFF stimulation, patients with PD‐ON stimulation performed comparably to controls. The memory tasks were executed with normal error rates in PD‐ON and ‐OFF stimulation. In contrast to these behavioral results, whether the corresponding prefrontal activation was differentially affected by deep brain stimulation status in patients depended on whether the WM modality was SP versus NSP. Thus, SP WM was associated with (1) abnormal reduction in dorsolateral prefrontal activity in PD‐OFF and ‐ON stimulation and (2) abnormal overactivation in parieto‐temporal cortex in PD‐OFF and in limbic circuits in PD‐ON stimulation. In NSP WM, normal activation of the ventral prefrontal cortex was restored in PD‐ON stimulation. In both visual modalities the posterior cerebral regions including fusiform cortex and cerebellum, displayed abnormally reduced activity in PD. These results indicate that PD induces a prefrontal hypoactivation that STN stimulation can partially restore in a modality selective manner by additional recruitment of limbic structures in SP WM or by recovery of the ventral prefrontal activation in NSP WM. Hum Brain Mapp 35:552–566, 2014. © 2012 Wiley Periodicals, Inc.     

Disturbed functional connectivity within brain networks subserving domain-specific subcomponents of working memory in schizophrenia: Relation to performance and clinical symptoms

Introduction

Disturbed interregional functional connectivity has been hypothesized to be a promising marker of schizophrenia. The relationship between working memory (WM) impairment, disturbed functional connectivity, and the characteristic symptoms of schizophrenia, however, remains elusive.

Methods

We used functional MRI (fMRI) to investigate in patients with schizophrenia and matched controls the patterns of functional connectivity during the performance of different tasks selectively engaging subcomponent processes of working memory.

Results

Compared with controls, patients showed reduced connectivity of the prefrontal cortex with the intraparietal cortex and the hippocampus and abnormal negative interactions between the ventrolateral and dorsolateral prefrontal cortex during the non-articulatory maintenance of phonological information. During the maintenance of visuospatial information, patients presented reduced connectivity between regions in the superior parietal and occipital cortex, as well as enhanced positive connectivity of the frontal eye field with visual processing areas.

Discussion

Our findings suggest complex dysregulations within the networks supporting working memory functions in schizophrenia, which manifest as decreased positive and abnormal negative interactions. Correlations between the connection strength and WM performance suggest that these dysregulations may be neurofunctional correlates of the WM deficits seen in schizophrenia. Altered prefronto-hippocampal and parieto-occipital connectivity was further found to be associated with higher positive symptoms, providing a possible explanation for the development of delusions and disorganization symptoms.

Conclusion

The present findings can help to better understand the relationship between altered patterns of synchronized brain activity and the cognitive and clinical symptoms of schizophrenia.     

Modulation of neural oscillations during working memory update,maintenance, and readout: An hdEEG study

Working memory (WM) performance is very often measured using the n‐back task, in which the participant is presented with a sequence of stimuli, and required to indicate whether the current stimulus matches the one presented n steps earlier. In this study, we used high‐density electroencephalography (hdEEG) coupled to source localization to obtain information on spatial distribution and temporal dynamics of neural oscillations associated with WM update, maintenance and readout. Specifically, we a priori selected regions from a large fronto‐parietal network, including also the insula and the cerebellum, and we analyzed modulation of neural oscillations by event‐related desynchronization and synchronization (ERD/ERS). During update and readout, we found larger θ ERS and smaller β ERS respect to maintenance in all the selected areas. γ_LOW and γ_HIGH bands oscillations decreased in the frontal and insular cortices of the left hemisphere. In the maintenance phase we observed decreased θ oscillations and increased β oscillations (ERS) in most of the selected posterior areas and focally increased oscillations in γ_LOW and γ_HIGH bands in the frontal and insular cortices of the left hemisphere. Finally, during WM readout, we also found a focal modulation of the γ_LOW band in the left fusiform cortex and cerebellum, depending on the response trial type (true positive vs. true negative). Overall, our study demonstrated specific spectral signatures associated with updating of memory information, WM maintenance, and readout, with relatively high spatial resolution.     

Associations between sleep duration trajectories from adolescence to early adulthood and working memory,schooling and income: a prospective birth cohort study from Brazil

ObjectiveThis study aimed to evaluate the relationship between sleep duration trajectories from adolescence to early adulthood and working memory, schooling and income at 22 years in the Pelotas 1993 Birth Cohort.MethodsSleep duration was self-reported at ages 11, 18 and 22. Sleep trajectories were identified using finite mixture models. Schooling was recorded as the number of completed years of education. Working memory was evaluated using The Digit Span test and income was recorded for who reported have a job and received a payment for this in the previous month. All analyses were stratified by sex.ResultsWe used crude and adjusted (for demographic, health and behavior characteristics measured at perinatal and 11-years) linear or quantile regression analyses. A total of 2915 individuals were included. Three trajectories for males were used: “increase and maintenance” (3.4%), “fast reduction and maintenance” (45.0%) and “constant reduction” (51.6%). For females, we used the trajectories: “increase and decrease” (2.4%), “fast reduction and maintenance” (25.6%) and “constant reduction” (72.0%). Males from “increase and maintenance” and females from “increase and decrease” trajectories scored, on average, 1.6 and 1.8 points lower, respectively, in working memory test. They presented a median of 1.4 and 2.6 fewer schooling years, respectively, compared to individuals from the “fast reduction and maintenance” trajectory. Regarding income, no significant association was observed.ConclusionSleep duration during adolescence could affect cognitive and educational outcomes in early adulthood. Individuals who presented the expected sleep trajectory (decrease of sleep duration across adolescence) presented better outcomes.     

Cortical and subcortical responsiveness to intensive adaptive working memory training: An MRI surface‐based analysis

Working memory training (WMT) has been shown to have effects on cognitive performance, the precise effects and the underlying neurobiological mechanisms are, however, still a matter of debate. In particular, the impact of WMT on gray matter morphology is still rather unclear. In the present study, 59 healthy middle‐aged participants (age range 50–65 years) were pseudo‐randomly single‐blinded allocated to an 8‐week adaptive WMT or an 8‐week nonadaptive intervention. Before and after the intervention, high resolution magnetic resonance imaging (MRI) was performed and cognitive test performance was assessed in all participants. Vertex‐wise cortical volume, thickness, surface area, and cortical folding was calculated. Seven subcortical volumes of interest and global mean cortical thickness were also measured. Comparisons of symmetrized percent change (SPC) between groups were conducted to identify group by time interactions. Greater increases in cortical gyrification in bilateral parietal regions, including superior parietal cortex and inferior parietal lobule as well as precuneus, greater increases in cortical volume and thickness in bilateral primary motor cortex, and changes in surface area in bilateral occipital cortex (medial and lateral occipital cortex) were detected in WMT group after training compared to active controls. Structural training‐induced changes in WM‐related regions, especially parietal regions, might provide a better brain processing environment for higher WM load.