Differential neural activity in the recognition of old versus new events: An Activation Likelihood Estimation Meta‐Analysis

This study presents a meta‐analysis comparing hit and correct rejection (CR) conditions across 48 fMRI studies. Old/new (hit > CR) effects associated most consistently with (1) components of the default‐mode network, including the left angular gyrus, bilateral precuneus, and bilateral posterior cingulate regions, which may support the mental re‐experiencing of an old event, or ecphory; (2) components of the cognitive‐control network, involving the left dorsolateral and dorsomedial prefrontal cortex and bilateral intraparietal sulcus regions, which may mediate memory and non‐memory control functions; and (3) the caudate nucleus, a key part of the brain's reward system that may support the satisfaction tied to target‐detection. Direct comparisons of old/new effects between item versus source retrieval and “remember” versus “know” retrieval yielded three main sets of findings. First, default‐mode network regions showed greater old/new effects in conditions associated with richer ecphoric processing. Second, cognitive‐control network regions showed greater old/new effects in conditions associated with a greater demand for strategic‐retrieval processing. Third, the caudate nucleus showed greater old/new effects in conditions tied to greater confidence in target‐detection. New/old (CR > hit) effects most strongly associated with the bilateral medial temporal lobe, possibly reflecting greater encoding‐related activity for new than for old items, and the right posterior middle temporal regions, possibly reflecting repetition‐related neural priming for old items. In conclusion, neural activity distinguishing old from new events comprises an ensemble of multiple memory‐specific activities, including encoding, retrieval, and priming, as well as multiple types of more general cognitive activities, including default‐mode, cognitive‐control, and reward processing. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.     

The neuropsychology of autobiographical memory

This special issue of Cortex focuses on the relative contribution of different neural networks to memory and the interaction of ‘core' memory processes with other cognitive processes. In this article, we examine both. Specifically, we identify cognitive processes other than encoding and retrieval that are thought to be involved in memory; we then examine the consequences of damage to brain regions that support these processes. This approach forces a consideration of the roles of brain regions outside of the frontal, medial- temporal, and diencephalic regions that form a central part of neurobiological theories of memory. Certain kinds of damage to visual cortex or lateral temporal cortex produced impairments of visual imagery or semantic memory; these patterns of impairment are associated with a unique pattern of amnesia that was distinctly different from the pattern associated with medial-temporal trauma. On the other hand, damage to language regions, auditory cortex, or parietal cortex produced impairments of language, auditory imagery, or spatial imagery; however, these impairments were not associated with amnesia. Therefore, a full model of autobiographical memory must consider cognitive processes that are not generally considered ‘core processes,' as well as the brain regions upon which these processes depend.     

Numerical working memory alters alpha‐beta oscillations and connectivity in the parietal cortices

Although the neural bases of numerical processing and memory have been extensively studied, much remains to be elucidated concerning the spectral and temporal dynamics surrounding these important cognitive processes. To further this understanding, we employed a novel numerical working memory paradigm in 28 young, healthy adults who underwent magnetoencephalography (MEG). The resulting data were examined in the time‐frequency domain prior to image reconstruction using a beamformer. Whole‐brain, spectrally‐constrained coherence was also employed to determine network connectivity. In response to the numerical task, participants exhibited robust alpha/beta oscillations in the bilateral parietal cortices. Whole‐brain statistical comparisons examining the effect of numerical manipulation during memory‐item maintenance revealed a difference centered in the right superior parietal cortex, such that oscillatory responses during numerical manipulation were significantly stronger than when no manipulation was necessary. Additionally, there was significantly reduced cortico‐cortical coherence between the right and left superior parietal regions during the manipulation compared to the maintenance trials, indicating that these regions were functioning more independently when the numerical information had to be actively processed. In sum, these results support previous studies that have implicated the importance of parietal regions in numerical processing, but also provide new knowledge on the spectral, temporal, and network dynamics that serve this critical cognitive function during active working memory maintenance.     

Brain‐derived neurotrophic factor val66met polymorphism and hippocampal activation during episodic encoding and retrieval tasks

Brain‐derived neurotrophic factor (BDNF) is a neurotrophin which has been shown to regulate cell survival and proliferation, as well as synaptic growth and hippocampal long‐term potentiation. A naturally occurring single nucleotide polymorphism in the human BDNF gene (val66met) has been associated with altered intercellular trafficking and regulated secretion of BDNF in met compared to val carriers. Additionally, previous studies have found a relationship between the BDNF val66met genotype and functional activity in the hippocampus during episodic and working memory tasks in healthy young adults. Specifically, studies have found that met carriers exhibit both poorer performance and reduced neural activity within the medial temporal lobe (MTL) when performing episodic memory tasks. However, these studies have not been well replicated and have not considered the role of behavioral differences in the interpretation of neural differences. The current study sought to control for cognitive performance in investigating the role of the BDNF val66met genotype on neural activity associated with episodic memory. Across item and relational memory tests, met carriers exhibited increased MTL activation during both encoding and retrieval stages, compared to noncarriers. The results suggest that met carriers are able to recruit MTL activity to support successful memory processes, and reductions in cognitive performance observed in prior studies are not a ubiquitous effect associated with variants of the BDNF val66met genotype. © 2010 Wiley‐Liss, Inc.     

Abnormal neural response to phonological working memory demands in persistent developmental stuttering

Persistent developmental stuttering is a neurological disorder that commonly manifests as a motor problem. Cognitive theories, however, hold that poorly developed cognitive skills are the origins of stuttering. Working memory (WM), a multicomponent cognitive system that mediates information maintenance and manipulation, is known to play an important role in speech production, leading us to postulate that the neurophysiological mechanisms underlying stuttering may be associated with a WM deficit. Using functional magnetic resonance imaging, we aimed to elucidate brain mechanisms in a phonological WM task in adults who stutter and controls. A right‐lateralized compensatory mechanism for a deficit in the rehearsal process and neural disconnections associated with the central executive dysfunction were found. Furthermore, the neural abnormalities underlying the phonological WM were independent of memory load. This study demonstrates for the first time the atypical neural responses to phonological WM in PWS, shedding new light on the underlying cause of stuttering.     

Oscillatory multiplexing of neural population codes for interval timing and working memory

Interval timing and working memory are critical components of cognition that are supported by neural oscillations in prefrontal–striatal–hippocampal circuits. In this review, the properties of interval timing and working memory are explored in terms of behavioral, anatomical, pharmacological, and neurophysiological findings. We then describe the various neurobiological theories that have been developed to explain these cognitive processes – largely independent of each other. Following this, a coupled excitatory – inhibitory oscillation (EIO) model of temporal processing is proposed to address the shared oscillatory properties of interval timing and working memory. Using this integrative approach, we describe a hybrid model explaining how interval timing and working memory can originate from the same oscillatory processes, but differ in terms of which dimension of the neural oscillation is utilized for the extraction of item, temporal order, and duration information. This extension of the striatal beat-frequency (SBF) model of interval timing (Matell and Meck, 2000, Matell and Meck, 2004) is based on prefrontal–striatal–hippocampal circuit dynamics and has direct relevance to the pathophysiological distortions observed in time perception and working memory in a variety of psychiatric and neurological conditions.     

Factors that influence the relative use of multiple memory systems

Neurobehavioral evidence supports the existence of at least two anatomically distinct “memory systems” in the mammalian brain that mediate dissociable types of learning and memory; a “cognitive” memory system dependent upon the hippocampus and a “stimulus‐response/habit” memory system dependent upon the dorsolateral striatum. Several findings indicate that despite their anatomical and functional distinctiveness, hippocampal‐ and dorsolateral striatal‐dependent memory systems may potentially interact and that, depending on the learning situation, this interaction may be cooperative or competitive. One approach to examining the neural mechanisms underlying these interactions is to consider how various factors influence the relative use of multiple memory systems. The present review examines several such factors, including information compatibility, temporal sequence of training, the visual sensory environment, reinforcement parameters, emotional arousal, and memory modulatory systems. Altering these parameters can lead to selective enhancements of either hippocampal‐dependent or dorsolateral striatal‐dependent memory, and bias animals toward the use of either cognitive or habit memory in dual‐solution tasks that may be solved adequately with either memory system. In many learning situations, the influence of such experimental factors on the relative use of memory systems likely reflects a competitive interaction between the systems. Research examining how various factors influence the relative use of multiple memory systems may be a useful method for investigating how these systems interact with one another. © 2013 Wiley Periodicals, Inc.     

Functional connectivity in category‐selective brain networks after encoding predicts subsequent memory

Activity in category selective regions of the temporal and parietal lobes during encoding has been associated with subsequent memory for face and scene stimuli. Reactivation theories of memory consolidation predict that after encoding connectivity between these category‐selective regions and the hippocampus should be modulated and predict recognition memory. However, support for this proposal has been limited in humans. Here, participants completed a resting‐state functional MRI (fMRI) scan, followed by face‐ and place‐encoding tasks, followed by another resting‐state fMRI scan during which they were asked to think about the stimuli they had previously encountered. Individual differences in face recognition memory were predicted by the degree to which connectivity between face‐responsive regions of the fusiform gyrus and perirhinal cortex increased following the face‐encoding task. In contrast, individual differences in scene recognition were predicted by connectivity between the hippocampus and a scene‐selective region of the retrosplenial cortex before and after the place‐encoding task. Our results provide novel evidence for category specificity in the neural mechanisms supporting memory consolidation.     

Distinct neural substrates for visual short‐term memory of actions

Fundamental theories of human cognition have long posited that the short‐term maintenance of actions is supported by one of the “core knowledge” systems of human visual cognition, yet its neural substrates are still not well understood. In particular, it is unclear whether the visual short‐term memory (VSTM) of actions has distinct neural substrates or, as proposed by the spatio‐object architecture of VSTM, shares them with VSTM of objects and spatial locations. In two experiments, we tested these two competing hypotheses by directly contrasting the neural substrates for VSTM of actions with those for objects and locations. Our results showed that the bilateral middle temporal cortex (MT) was specifically involved in VSTM of actions because its activation and its functional connectivity with the frontal–parietal network (FPN) were only modulated by the memory load of actions, but not by that of objects/agents or locations. Moreover, the brain regions involved in the maintenance of spatial location information (i.e., superior parietal lobule, SPL) was also recruited during the maintenance of actions, consistent with the temporal–spatial nature of actions. Meanwhile, the frontoparietal network (FPN) was commonly involved in all types of VSTM and showed flexible functional connectivity with the domain‐specific regions, depending on the current working memory tasks. Together, our results provide clear evidence for a distinct neural system for maintaining actions in VSTM, which supports the core knowledge system theory and the domain‐specific and domain‐general architectures of VSTM.     

Update on temporal lobe‐dependent information processing,in health and disease

The past decade has been characterized by a lot of remodeling in the field of learning and memory. Both of them, often associated with neuronal oscillations, an emergent property of brain networks, are governed by temporal lobe (TL) functional connectivity. An impairment of oscillatory mechanisms indeed often leads to TL‐dependent cognitive deficits. While the classical view assigned the TL a major role in spatial information processing, new theories rather confer to the TL a more general function in cognitive processes beyond space representation. The present review covers, both in humans and in animal models, (a) the updated role of the TL in cognitive processes, addressing current debates in the field and proposing a scenario on how TL structures cooperate in order to bind an integrated representation of afferent information, (b) the oscillatory mechanisms underlying these TL‐dependent cognitive functions (theta, gamma, sharp wave ripples) and (c) how TL‐dependent cognition is altered during temporal lobe epilepsy, proposing a scenario on how reorganized TL networks in TLE leads to rhythmopathies and cognitive deficits. Temporal lobe epilepsy (TLE) is a well‐studied neurological disease. Patients do not only suffer from epileptic seizures but also from cognitive and behavioral deficits between their seizures called comorbidities. TLE animal models are therefore used to understand how and when these comorbidities arise and what their underlying mechanisms are.     

BRAIN LOCALIZATION OF MEMORY CHUNKS IN CHESSPLAYERS

Chess experts store domain-specific representations in their long-term memory; due to the activation of such representations, they perform with high accuracy in tasks that require the maintenance of previously seen information. Chunk-based theories of expertise (chunking theory: ; template theory: ) state that expertise is acquired mainly by the acquisition and storage in long-term memory of familiar chunks that allow quick recognition. This study tested some predictions of these theories by using fMRI while chessplayers performed a recognition memory task. These theories predict that chessplayers access long-term memory chunks of domain-specific information, which are presumably stored in the temporal lobes. It was also predicted that the recognition memory tasks would activate working memory areas in the frontal and parietal lobes. These predictions were supported by the data.     

Rest boosts the long‐term retention of spatial associative and temporal order information

People retain more new verbal episodic information for at least 7 days if they rest for a few minutes after learning than if they attend to new information. It is hypothesized that rest allows for superior consolidation of new memories. In rodents, rest periods promote hippocampal replay of a recently travelled route, and this replay is thought to be critical for memory consolidation and subsequent spatial navigation. If rest boosts human memory by promoting hippocampal replay/consolidation, then the beneficial effect of rest should extend to complex (hippocampal) memory tasks, for example, tasks probing associations and sequences. We investigated this question via a virtual reality route memory task. Healthy young participants learned two routes to a 100% criterion. One route was followed by a 10‐min rest and the other by a 10‐min spot the difference game. For each learned route, participants performed four delayed spatial memory tests probing: (i) associative (landmark‐direction) memory, (ii) cognitive map formation, (iii) temporal (landmark) order memory, and (iv) route memory. Tests were repeated after 7 days to determine any long‐term effects. No effect of rest was detected in the route memory or cognitive map tests, most likely due to ceiling and floor effects, respectively. Rest did, however, boost retention in the associative memory and temporal order memory tests, and this boost remained for at least 7 days. We therefore demonstrate that the benefit of rest extends to (spatial) associative and temporal order memory in humans. We hypothesise that rest allows superior consolidation/hippocampal replay of novel information pertaining to a recently learned route, thus boosting new memories over the long term. © 2015 Wiley Periodicals, Inc.     

Cerebellar contributions to verbal working memory: beyond cognitive theory

Neuropsychological findings together with recent advances in neuroanatomical and neuroimaging techniques have spurred the investigation of cerebellar contributions to cognition. One cognitive process that has been the focus of much research is working memory, in particular its verbal component. Influenced by Baddeley’s cognitive theory of working memory, cerebellar activation during verbal working memory tasks has been predominantly attributed to the cerebellum’s involvement in an articulatory rehearsal network. Recent neuroimaging and neuropsychological findings are inconsistent with a simple motor view of the cerebellum’s function in verbal working memory. The present article examines these findings and their implications for an articulatory rehearsal proposal of cerebellar function. Moving beyond cognitive theory, we propose two alternative explanations for cerebellar involvement in verbal working memory: Error-driven adjustment and internal timing. These general theories of cerebellar function have been successfully adapted from the motor literature to explain cognitive functions of the cerebellum. We argue that these theories may also provide a useful framework to understand the non-motor contributions of the cerebellum to verbal working memory.     

Rapid improvement of cognitive maps in the awake state

Post‐navigation awake quiescence, relative to task engagement, benefits the accuracy of a new “cognitive map”. This effect is hypothesized to reflect awake quiescence, like sleep, being conducive to the consolidation and integration of new spatial memories. Sleep has been shown to improve cognitive map accuracy over time. It remained unknown whether awake quiescence can induce similar time‐related improvements in new cognitive maps, or whether it simply counteracts their decay. We examined this question via two experiments. In Experiment 1, using an established cognitive mapping paradigm, we reveal that map accuracy for a virtual town was significantly better in people whose memory was probed after 10 min of post‐navigation awake quiescence or ongoing cognitive engagement, relative to those whose memory was probed shortly after initial navigation. In Experiment 2, using a newly developed cognitive mapping task that involved a more complex and real‐life virtual town, we again found that map accuracy was superior in those whose memory was probed after 10 min of awake quiescence than those who were tested soon after navigation. These findings indicate that actual improvements in human memories are not restricted to sleep. Thus, contrary to conventional wisdom and theories, the passage of (day)time need not always result in forgetting.     

Human declarative memory formation: segregating rhinal and hippocampal contributions

The medial temporal lobe (MTL) is the core structure of the declarative memory system, but which specific operation is performed by anatomically defined MTL substructures? One hypothesis proposes that the hippocampus carries out an exclusively mnemonic operation during declarative memory formation that is insensitive to content, whereas the rhinal cortex carries out an operation supporting memory formation indirectly. To explore the interaction between a salient item feature and memory formation, we contrasted neural correlates of memory formation of high‐ and low‐frequency words. Event‐related potentials (ERPs) were recorded via depth electrodes from within the MTL in nine epilepsy patients while they memorized single words. To assess memory formation, ERPs to words subsequently recalled in a free recall test were contrasted with ERPs to forgotten words. More high‐ than low‐frequency words were remembered. High‐frequency words led to distinct ERP subsequent memory effects in rhinal cortex and hippocampus. Low‐frequency words, however, were only associated with the hippocampal ERP effect. The anatomically restricted interaction between word frequency and memory formation might indicate a semantically affected operation in the parahippocampal region supporting memory formation indirectly. By contrast, the missing interaction in hippocampal recordings might suggest a direct correlate of declarative memory formation that is insensitive to item properties. Hippocampus 2002;12:514–519. © 2002 Wiley‐Liss, Inc.     

The functional neuroanatomy of autobiographical memory: a meta-analysis

Autobiographical memory (AM) entails a complex set of operations, including episodic memory, self-reflection, emotion, visual imagery, attention, executive functions, and semantic processes. The heterogeneous nature of AM poses significant challenges in capturing its behavioral and neuroanatomical correlates. Investigators have recently turned their attention to the functional neuroanatomy of AM. We used the effect-location method of meta-analysis to analyze data from 24 functional imaging studies of AM. The results indicated a core neural network of left-lateralized regions, including the medial and ventrolateral prefrontal, medial and lateral temporal and retrosplenial/posterior cingulate cortices, the temporoparietal junction and the cerebellum. Secondary and tertiary regions, less frequently reported in imaging studies of AM, are also identified. We examined the neural correlates of putative component processes in AM, including, executive functions, self-reflection, episodic remembering and visuospatial processing. We also separately analyzed the effect of select variables on the AM network across individual studies, including memory age, qualitative factors (personal significance, level of detail and vividness), semantic and emotional content, and the effect of reference conditions. We found that memory age effects on medial temporal lobe structures may be modulated by qualitative aspects of memory. Studies using rest as a control task masked process-specific components of the AM neural network. Our findings support a neural distinction between episodic and semantic memory in AM. Finally, emotional events produced a shift in lateralization of the AM network with activation observed in emotion-centered regions and deactivation (or lack of activation) observed in regions associated with cognitive processes.     

Examining the development of memory for temporal context and its underlying neural processes using event-related potentials

Time is a critical feature of episodic memory—memory for events from a specific time and place (Tulving, 1972). Previous research indicates that temporal memory (memory for ‘when’) is slower to develop than memory for other details (e.g., ‘what’ and ‘where’), with improvements observed across middle and late childhood. The factors that drive these changes are not yet clear. We used an event-related potential (ERP) recognition memory paradigm to investigate the underlying processes of memory for temporal context in middle to late childhood (7−9-year-olds; 10−12-year-olds) and young adulthood. Behaviorally, we observed age-related improvements in the ability to place events in temporal context. ERP analyses showed old/new effects for children and adults. We also found brain-behavior relations for 1) episodic memory (ERP mean amplitude difference between source hits and correctly identified new trials was correlated to behavioral accuracy), and 2) temporal memory (ERP mean amplitude difference between source hits and source error trials was correlated to accuracy of temporal memory judgments). This work furthers our understanding of the cognitive processes and neural signatures supporting temporal memory development in middle to late childhood, and has implications for episodic memory development more broadly.     

A single‐trace dual‐process model of episodic memory: A novel computational account of familiarity and recollection

Dual‐process theories of episodic memory state that retrieval is contingent on two independent processes: familiarity (providing a sense of oldness) and recollection (recovering events and their context). A variety of studies have reported distinct neural signatures for familiarity and recollection, supporting dual‐process theory. One outstanding question is whether these signatures reflect the activation of distinct memory traces or the operation of different retrieval mechanisms on a single memory trace. We present a computational model that uses a single neuronal network to store memory traces, but two distinct and independent retrieval processes access the memory. The model is capable of performing familiarity and recollection‐based discrimination between old and new patterns, demonstrating that dual‐process models need not to rely on multiple independent memory traces, but can use a single trace. Importantly, our putative familiarity and recollection processes exhibit distinct characteristics analogous to those found in empirical data; they diverge in capacity and sensitivity to sparse and correlated patterns, exhibit distinct ROC curves, and account for performance on both item and associative recognition tests. The demonstration that a single‐trace, dual‐process model can account for a range of empirical findings highlights the importance of distinguishing between neuronal processes and the neuronal representations on which they operate. © 2009 Wiley‐Liss, Inc.     

Functional connectivity of hippocampal and prefrontal networks during episodic and spatial memory based on real‐world environments

Several recent studies have compared episodic and spatial memory in neuroimaging paradigms in order to understand better the contribution of the hippocampus to each of these tasks. In the present study, we build on previous findings showing common neural activation in default network areas during episodic and spatial memory tasks based on familiar, real‐world environments (Hirshhorn et al. (2012) Neuropsychologia 50:3094–3106). Following previous demonstrations of the presence of functionally connected sub‐networks within the default network, we performed seed‐based functional connectivity analyses to determine how, depending on the task, the hippocampus and prefrontal cortex differentially couple with one another and with distinct whole‐brain networks. We found evidence for a medial prefrontal‐parietal network and a medial temporal lobe network, which were functionally connected to the prefrontal and hippocampal seeds, respectively, regardless of the nature of the memory task. However, these two networks were functionally connected with one another during the episodic memory task, but not during spatial memory tasks. Replicating previous reports of fractionation of the default network into stable sub‐networks, this study also shows how these sub‐networks may flexibly couple and uncouple with one another based on task demands. These findings support the hypothesis that episodic memory and spatial memory share a common medial temporal lobe‐based neural substrate, with episodic memory recruiting additional prefrontal sub‐networks. © 2014 Wiley Periodicals, Inc.     

Mild Thyrotoxicosis Leads to Brain Perfusion Changes: An Arterial Spin Labelling Study

Hypo‐ and hyperthyroidism have effects on brain structure and function, as well as cognitive processes, including memory. However, little is known about the influence of thyroid hormones on brain perfusion and the relationship of such perfusion changes with cognition. The present study aimed to demonstrate the effect of short‐term experimental hyperthyroidism on brain perfusion in healthy volunteers and to assess whether perfusion changes, if present, are related to cognitive performance. It is known that an interaction exists between brain perfusion and cerebral oxygen consumption rate and it is considered that neural activation increases cerebral regional perfusion rate in brain areas associated with memory. Measuring cerebral blood flow may therefore represent a proxy for neural activity. Therefore, arterial spin labelling (ASL) measurements were conducted and later analysed to evaluate brain perfusion in 29 healthy men before and after ingesting thyroid hormones for 8 weeks. Psychological tests concerning memory were performed at the same time‐points and the results were correlated with the imaging results. In the hyperthyroid condition, perfusion was increased in the posterior cerebellum in regions connected with cerebral networks associated with cognitive control and the visual cortex compared to the euthyroid condition. In addition, these perfusion changes were positively correlated with changes of performance in the German version of the Auditory Verbal Learning Task [AVLT, Verbaler Lern‐und‐Merkfähigkeits‐Test (VLMT)]. Cerebellar perfusion and function therefore appears to be modulated by thyroid hormones, likely because the cerebellum hosts a high number of thyroid hormone receptors.