Hippocampal Functions Modulate Transfer-Appropriate Cortical Representations Supporting Subsequent Memory.

The hippocampus plays a central role as a coordinate system or index of information stored in neocortical loci. Nonetheless, it remains unclear how hippocampal processes integrate with cortical information to facilitate successful memory encoding. Thus, the goal of the current study was to identify specific hippocampal-cortical interactions that support object encoding. We collected fMRI data while 19 human participants (7 female and 12 male) encoded images of real-world objects and tested their memory for object concepts and image exemplars (i.e., conceptual and perceptual memory). Representational similarity analysis revealed robust representations of visual and semantic information in canonical visual (e.g., occipital cortex) and semantic (e.g., angular gyrus) regions in the cortex, but not in the hippocampus. Critically, hippocampal functions modulated the mnemonic impact of cortical representations that are most pertinent to future memory demands, or transfer-appropriate representations Subsequent perceptual memory was best predicted by the strength of visual representations in ventromedial occipital cortex in coordination with hippocampal activity and pattern information during encoding. In parallel, subsequent conceptual memory was best predicted by the strength of semantic representations in left inferior frontal gyrus and angular gyrus in coordination with either hippocampal activity or semantic representational strength during encoding. We found no evidence for transfer-incongruent hippocampal-cortical interactions supporting subsequent memory (i.e., no hippocampal interactions with cortical visual/semantic representations supported conceptual/perceptual memory). Collectively, these results suggest that diverse hippocampal functions flexibly modulate cortical representations of object properties to satisfy distinct future memory demands.Significance Statement The hippocampus is theorized to index pieces of information stored throughout the cortex to support episodic memory. Yet how hippocampal processes integrate with cortical representation of stimulus information remains unclear. Using fMRI, we examined various forms of hippocampal-cortical interactions during object encoding in relation to subsequent performance on conceptual and perceptual memory tests. Our results revealed novel hippocampal-cortical interactions that utilize semantic and visual representations in transfer-appropriate manners: conceptual memory supported by hippocampal modulation of frontoparietal semantic representations, and perceptual memory supported by hippocampal modulation of occipital visual representations. These findings provide important insights into the neural mechanisms underlying the formation of information-rich episodic memory and underscore the value of studying the flexible interplay between brain regions for complex cognition.

Visual Recognition Memory of Scenes Is Driven by Categorical, Not Sensory, Visual Representations.

When we perceive a scene, our brain processes various types of visual information simultaneously, ranging from sensory features, such as line orientations and colors, to categorical features, such as objects and their arrangements. Whereas the role of sensory and categorical visual representations in predicting subsequent memory has been studied using isolated objects, their impact on memory for complex scenes remains largely unknown. To address this gap, we conducted an fMRI study in which female and male participants encoded pictures of familiar scenes (e.g., an airport picture) and later recalled them, while rating the vividness of their visual recall. Outside the scanner, participants had to distinguish each seen scene from three similar lures (e.g., three airport pictures). We modeled the sensory and categorical visual features of multiple scenes using both early and late layers of a deep convolutional neural network. Then, we applied representational similarity analysis to determine which brain regions represented stimuli in accordance with the sensory and categorical models. We found that categorical, but not sensory, representations predicted subsequent memory. In line with the previous result, only for the categorical model, the average recognition performance of each scene exhibited a positive correlation with the average visual dissimilarity between the item in question and its respective lures. These results strongly suggest that even in memory tests that ostensibly rely solely on visual cues (such as forced-choice visual recognition with similar distractors), memory decisions for scenes may be primarily influenced by categorical rather than sensory representations.

Effects of Aging on Successful Object Encoding: Enhanced Semantic Representations Compensate for Impaired Visual Representations.

Although episodic memory and visual processing decline substantially with healthy aging, semantic knowledge is generally spared. There is evidence that older adults' spared semantic knowledge can support episodic memory. Here, we used functional magnetic resonance imaging (fMRI) combined with representational similarity analyses (RSAs) to examine how novel visual and preexisting semantic representations at encoding predict subjective memory vividness at retrieval. Eighteen young and seventeen older adults (female and male participants) encoded images of objects during fMRI scanning and recalled these images while rating the vividness of their memories. After scanning, participants discriminated between studied images and similar lures. RSA based on a deep convolutional neural network and normative concept feature data were used to link patterns of neural activity during encoding to visual and semantic representations. Relative to young adults, the specificity of activation patterns for visual features was reduced in older adults, consistent with dedifferentiation. However, the specificity of activation patterns for semantic features was enhanced in older adults, consistent with hyperdifferentiation. Despite dedifferentiation, visual representations in early visual cortex (EVC) predicted high memory vividness in both age groups. In contrast, semantic representations in lingual gyrus (LG) and fusiform gyrus (FG) were associated with high memory vividness only in the older adults. Intriguingly, data suggests that older adults with lower specificity of visual representations in combination with higher specificity of semantic representations tended to rate their memories as more vivid. Our findings suggest that memory vividness in aging relies more on semantic representations over anterior regions, potentially compensating for age-related dedifferentiation of visual information in posterior regions.SIGNIFICANCE STATEMENT Normal aging is associated with impaired memory for events while semantic knowledge might even improve. We investigated the effects of aging on the specificity of visual and semantic information in the brain when viewing common objects and how this information enables subsequent memory vividness for these objects. Using functional magnetic resonance imaging (fMRI) combined with modeling of the stimuli we found that visual information was represented with less specificity in older than young adults while still supporting memory vividness. In contrast semantic information supported memory vividness only in older adults and especially in those individuals that had the lowest specificity of visual information. These findings provide evidence for a spared semantic memory system increasingly recruited to compensate for degraded visual representations in older age.

Neural retrieval processes occur more rapidly for visual mental images that were previously encoded with high-vividness.

Visual mental imagery refers to our ability to experience visual images in the absence of sensory stimulation. Studies have shown that visual mental imagery can improve episodic memory. However, we have limited understanding of the neural mechanisms underlying this improvement. Using electroencephalography, we examined the neural processes associated with the retrieval of previously generated visual mental images, focusing on how the vividness at generation can modulate retrieval processes. Participants viewed word stimuli referring to common objects, forming a visual mental image of each word and rating the vividness of the mental image. This was followed by a surprise old/new recognition task. We compared retrieval performance for items rated as high- versus low-vividness at encoding. High-vividness items were retrieved with faster reaction times and higher confidence ratings in the memory judgment. While controlling for confidence, neural measures indicated that high-vividness items produced an earlier decrease in alpha-band activity at retrieval compared with low-vividness items, suggesting an earlier memory reinstatement. Even when low-vividness items were remembered with high confidence, they were not retrieved as quickly as high-vividness items. These results indicate that when highly vivid mental images are encoded, the speed of their retrieval occurs more rapidly, relative to low-vivid items.

The influence of imagery vividness and internally-directed attention on the neural mechanisms underlying the encoding of visual mental images into episodic memory.

Attention can be directed externally toward sensory information or internally toward self-generated information. Using electroencephalography (EEG), we investigated the attentional processes underlying the formation and encoding of self-generated mental images into episodic memory. Participants viewed flickering words referring to common objects and were tasked with forming visual mental images of the objects and rating their vividness. Subsequent memory for the presented object words was assessed using an old-new recognition task. Internally-directed attention during image generation was indexed as a reduction in steady-state visual evoked potentials (SSVEPs), oscillatory EEG responses at the frequency of a flickering stimulus. The results yielded 3 main findings. First, SSVEP power driven by the flickering word stimuli decreased as subjects directed attention internally to form the corresponding mental image. Second, SSVEP power returned to pre-imagery baseline more slowly for low- than high-vividness later remembered items, suggesting that longer internally-directed attention is required to generate subsequently remembered low-vividness images. Finally, the event-related-potential difference due to memory was more sustained for subsequently remembered low- versus high-vividness items, suggesting that additional conceptual processing may have been needed to remember the low-vividness visual images. Taken together, the results clarify the neural mechanisms supporting the encoding of self-generated information.

Prediction error minimization as a common computational principle for curiosity and creativity.

We propose expanding the authors' shared novelty-seeking basis for creativity and curiosity by emphasizing an underlying computational principle: Minimizing prediction errors (mismatch between predictions and incoming data). Curiosity is tied to the anticipation of minimizing prediction errors through future, novel information, whereas creative AHA moments are connected to the actual minimization of prediction errors through current, novel information.

Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

Cognitive ageing research examines the cognitive abilities that are preserved and/or those that decline with advanced age. There is great individual variability in cognitive ageing trajectories. Some older adults show little decline in cognitive ability compared with young adults and are thus termed 'optimally ageing'. By contrast, others exhibit substantial cognitive decline and may develop dementia. Human neuroimaging research has led to a number of important advances in our understanding of the neural mechanisms underlying these two outcomes. However, interpreting the age-related changes and differences in brain structure, activation and functional connectivity that this research reveals is an ongoing challenge. Ambiguous terminology is a major source of difficulty in this venture. Three terms in particular - compensation, maintenance and reserve - have been used in a number of different ways, and researchers continue to disagree about the kinds of evidence or patterns of results that are required to interpret findings related to these concepts. As such inconsistencies can impede progress in both theoretical and empirical research, here, we aim to clarify and propose consensual definitions of these terms.

Author Correction: Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

In the originally published version of article, there were two errors in the references. The reference "Nilsson, J. & Lövdén, M. Naming is not explaining: future directions for the "cognitive reserve" and "brain maintenance" theories. Alzheimer's Res. Ther. 10, 34 (2018)" was missing. This reference has been added as REF. 14 in the HTML and PDF versions of the article and cited at the end of the sentence "However, over the years, these terms have been used inconsistently, creating confusion and slowing progress." on page 701 and at the end of the sentence "If reserve is defined merely as the factor that individuals with greater reserve have and then this factor is used to explain why some individuals have greater reserve, the argument is clearly circular." on page 704. The reference list has been renumbered accordingly. In addition, in the original reference list, REF. 91 was incorrect. The reference should have read "Cabeza, R. Hemispheric asymmetry reduction in older adults. The HAROLD model. Psychol. Aging 17, 85-100 (2002)". This reference, which is REF. 92 in the corrected reference list, has been corrected in the HTML and PDF versions of the article.

Publisher Correction: Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

In Figure 3b of the originally published article, the colours of the bars were incorrectly reversed. The bars shown in green should have been shown in blue to represent the findings from older adults, whereas the bars shown in blue should have been shown in green to represent the findings from young adults. This has been corrected in the HTML and PDF versions of the article. Images of the original figure are shown in the correction notice.

Assessing creativity independently of language: A language-independent remote associate task (LI-RAT).

Most creativity measures are either complex or language-dependent, hindering cross-cultural creativity assessment. We have therefore developed and tested a simple, language-independent insight task based on pictures in the style of the widely used verbal remote associate task (RAT). We demonstrate that the language-independent RAT (LI-RAT) allows assessment of different aspects of insight across large samples with different languages. It also correlates with other creativity and general problem-solving tasks. The entire stimulus set, including its preliminary normative data, is made freely available. This information can be used to select items based on accuracy, mean solution time, likelihood to produce an insight, or conceptual and perceptual similarity between the pictures per item.

Neural Mechanisms of Perceiving and Subsequently Recollecting Emotional Facial Expressions in Young and Older Adults.

It is known that emotional facial expressions modulate the perception and subsequent recollection of faces and that aging alters these modulatory effects. Yet, the underlying neural mechanisms are not well understood, and they were the focus of the current fMRI study. We scanned healthy young and older adults while perceiving happy, neutral, or angry faces paired with names. Participants were then provided with the names of the faces and asked to recall the facial expression of each face. fMRI analyses focused on the fusiform face area (FFA), the posterior superior temporal sulcus (pSTS), the OFC, the amygdala (AMY), and the hippocampus (HC). Univariate activity, multivariate pattern (MVPA), and functional connectivity analyses were performed. The study yielded two main sets of findings. First, in pSTS and AMY, univariate activity and MVPA discrimination during the processing of facial expressions were similar in young and older adults, whereas in FFA and OFC, MVPA discriminated facial expressions less accurately in older than young adults. These findings suggest that facial expression representations in FFA and OFC reflect age-related dedifferentiation and positivity effect. Second, HC-OFC connectivity showed subsequent memory effects (SMEs) for happy expressions in both age groups, HC-FFA connectivity exhibited SMEs for happy and neutral expressions in young adults, and HC-pSTS interactions displayed SMEs for happy expressions in older adults. These results could be related to compensatory mechanisms and positivity effects in older adults. Taken together, the results clarify the effects of aging on the neural mechanisms in perceiving and encoding facial expressions.

Visual and Semantic Representations Predict Subsequent Memory in Perceptual and Conceptual Memory Tests.

It is generally assumed that the encoding of a single event generates multiple memory representations, which contribute differently to subsequent episodic memory. We used functional magnetic resonance imaging (fMRI) and representational similarity analysis to examine how visual and semantic representations predicted subsequent memory for single item encoding (e.g., seeing an orange). Three levels of visual representations corresponding to early, middle, and late visual processing stages were based on a deep neural network. Three levels of semantic representations were based on normative observed ("is round"), taxonomic ("is a fruit"), and encyclopedic features ("is sweet"). We identified brain regions where each representation type predicted later perceptual memory, conceptual memory, or both (general memory). Participants encoded objects during fMRI, and then completed both a word-based conceptual and picture-based perceptual memory test. Visual representations predicted subsequent perceptual memory in visual cortices, but also facilitated conceptual and general memory in more anterior regions. Semantic representations, in turn, predicted perceptual memory in visual cortex, conceptual memory in the perirhinal and inferior prefrontal cortex, and general memory in the angular gyrus. These results suggest that the contribution of visual and semantic representations to subsequent memory effects depends on a complex interaction between representation, test type, and storage location.

Age-Related Compensatory Reconfiguration of PFC Connections during Episodic Memory Retrieval.

During demanding cognitive tasks, older adults (OAs) frequently show greater prefrontal cortex (PFC) activity than younger adults (YAs). This age-related increase in PFC activity is often associated with enhanced cognitive performance, suggesting functional compensation. However, the brain is a complex network of interconnected regions, and it is unclear how network connectivity of PFC regions differs for OAs versus YAs. To investigate this, we examined the age-related difference on the functional brain networks mediating episodic memory retrieval. YAs and OAs participants encoded and recalled visual scenes, and age-related differences in network topology during memory retrieval were investigated as a function of memory performance. We measured both changes in functional integration and reconfiguration in connectivity patterns. The study yielded three main findings. First, PFC regions were more functionally integrated with the rest of the brain network in OAs. Critically, this age-related increase in PFC integration was associated with better retrieval performance. Second, PFC regions showed stronger performance-related reconfiguration of connectivity patterns in OAs. Finally, the PFC reconfiguration increases in OAs tracked reconfiguration reductions in the medial temporal lobe (MTL)-a core episodic memory region, suggesting that PFC connectivity in OAs may be compensating for MTL deficits.

Between automatic and control processes: How relationships between problem elements interact to facilitate or impede insight.

Solving a problem requires relating the pieces of information available to each other and to the solution. We investigated how the strength of these relationships determines the likelihood of solving insight tasks based on remote associates. In these tasks, the solver is provided with several cues (e.g., drop, coat, summer) and has to find the solution that matches those cues (e.g., rain). We measured the semantic similarity between the cues and the solution (cue-solution similarity) as well as between cues (cue-cue similarity). We assume those relationships modulate two basic processes underlying insight problem-solving. First, there is an automatic activation process whereby conceptual activation spreads across a semantic network from each cue node to their associated nodes, potentially reaching the node of the solution. Thus, in general, the higher cue-solution similarity, the more likely the solution will be found (Prediction 1). Second, there is a controlled search process focused on an area in semantic space whose radius depends on competing cue-cue similarity. High cue-cue similarity will bias a search for the solution close to the provided cues because the associated nodes shared by both cues are highly coactivated. Therefore, high cue-cue similarity will have a beneficial effect when the cue-solution similarity is high but a detrimental effect when cue-solution similarity is low (Prediction 2). Our two predictions were confirmed using both verbal and pictorial remote association tasks, supporting the view that insight is dependent on an interaction of meaningful relationships between cues and solutions, and clarify the mechanisms of insight problem solving in remote associates.

Cortical Overlap and Cortical-Hippocampal Interactions Predict Subsequent True and False Memory.

The declarative memory system allows us to accurately recognize a countless number of items and events, particularly those strengthened by repeated exposure. However, increased familiarity due to repetition can also lead to false recognition of related but new items, particularly when mechanisms supporting fine-grain mnemonic discrimination fail. The hippocampus is thought to be particularly important in separating overlapping cortical inputs during encoding so that similar experiences can be differentiated. In the current study of male and female human subjects, we examine how neural pattern similarity between repeated exemplars of a given concept (e.g., apple) influences true and false memory for target or lure images. Consistent with past work, we found that subsequent true recognition was related to pattern similarity between concept exemplars and the entire encoding set (global encoding similarity), particularly in ventral visual stream. In addition, memory for an individual target exemplar (a specific apple) could be predicted solely by the degree of pattern overlap between the other exemplars (different apple pictures) of that concept (concept-specific encoding similarity). Critically, subsequent false memory for lures was mitigated when high concept-specific similarity in cortical areas was accompanied by differentiated hippocampal representations of the corresponding exemplars. Furthermore, both true and false memory entailed the reinstatement of concept-related information at varying levels of specificity. These results link both true and false memory to a measure of concept strength expressed in the overlap of cortical representations, and importantly, illustrate how the hippocampus serves to separate concurrent cortical overlap in the service of detailed memory.SIGNIFICANCE STATEMENT In some instances, the same processes that help promote memory for a general idea or concept can also hinder more detailed memory judgments, which may involve differentiating between closely related items. The current study shows that increased overlap in cortical representations for conceptually-related pictures is associated with increased recognition of repeated concept pictures. Whether similar lure items were falsely remembered as old further depended on the hippocampus, where the presence of more distinct representations protected against later false memory. This work suggests that the differentiability of brain patterns during perception is related to the differentiability of items in memory, but that fine-grain discrimination depends on the interaction between cortex and hippocampus.

Structural Controllability Predicts Functional Patterns and Brain Stimulation Benefits Associated with Working Memory.

The brain is an inherently dynamic system, and much work has focused on the ability to modify neural activity through both local perturbations and changes in the function of global network ensembles. Network controllability is a recent concept in network neuroscience that purports to predict the influence of individual cortical sites on global network states and state changes, thereby creating a unifying account of local influences on global brain dynamics. While this notion is accepted in engineering science, it is subject to ongoing debates in neuroscience as empirical evidence linking network controllability to brain activity and human behavior remains scarce. Here, we present an integrated set of multimodal brain-behavior relationships derived from fMRI, diffusion tensor imaging, and online repetitive transcranial magnetic stimulation (rTMS) applied during an individually calibrated working memory task performed by individuals of both sexes. The modes describing the structural network system dynamics showed direct relationships to brain activity associated with task difficulty, with difficult-to-reach modes contributing to functional brain states in the hard task condition. Modal controllability (a measure quantifying the contribution of difficult-to-reach modes) at the stimulated site predicted both fMRI activations associated with increasing task difficulty and rTMS benefits on task performance. Furthermore, fMRI explained 64% of the variance between modal controllability and the working memory benefit associated with 5 Hz online rTMS. These results therefore provide evidence toward the functional validity of network control theory, and outline a clear technique for integrating structural network topology and functional activity to predict the influence of stimulation on subsequent behavior.SIGNIFICANCE STATEMENT The network controllability concept proposes that specific cortical nodes are able to steer the brain into certain physiological states. By applying external perturbation to these control nodes, it is theorized that brain stimulation is able to selectively target difficult-to-reach states, potentially aiding processing and improving performance on cognitive tasks. The current study used rTMS and fMRI during a working memory task to test this hypothesis. We demonstrate that network controllability correlates with fMRI modulation because of working memory load and with the behavioral improvements that result from a multivisit intervention using 5 Hz rTMS. This study demonstrates the validity of network controllability and offers a new targeting approach to improve efficacy.

The visual and semantic features that predict object memory: Concept property norms for 1,000 object images.

Humans have a remarkable fidelity for visual long-term memory, and yet the composition of these memories is a longstanding debate in cognitive psychology. While much of the work on long-term memory has focused on processes associated with successful encoding and retrieval, more recent work on visual object recognition has developed a focus on the memorability of specific visual stimuli. Such work is engendering a view of object representation as a hierarchical movement from low-level visual representations to higher level categorical organization of conceptual representations. However, studies on object recognition often fail to account for how these high- and low-level features interact to promote distinct forms of memory. Here, we use both visual and semantic factors to investigate their relative contributions to two different forms of memory of everyday objects. We first collected normative visual and semantic feature information on 1,000 object images. We then conducted a memory study where we presented these same images during encoding (picture target) on Day 1, and then either a Lexical (lexical cue) or Visual (picture cue) memory test on Day 2. Our findings indicate that: (1) higher level visual factors (via DNNs) and semantic factors (via feature-based statistics) make independent contributions to object memory, (2) semantic information contributes to both true and false memory performance, and (3) factors that predict object memory depend on the type of memory being tested. These findings help to provide a more complete picture of what factors influence object memorability. These data are available online upon publication as a public resource.

The centrality of remembered moral and immoral actions in constructing personal identity.

There is a widespread belief that morally good traits and qualities are particularly central to psychological constructions of personal identity. People have a strong tendency to believe that they truly are morally good. We suggest that autobiographical memories of past events involving moral actions may inform how we come to believe that we are morally good. In two studies, we investigated the role of remembered past events involving moral and immoral actions in constructing perceived personal identity. For morally right actions only, we found that remembered actions judged to be more morally right relative to less morally right were more central to personal identity (Study 1). We then found that remembered morally right actions were more central to personal identity than remembered morally wrong actions (Study 2). We discuss these findings in relation to recent research on morality and personal identity.

Feedback-Based Learning in Aging: Contributions and Trajectories of Change in Striatal and Hippocampal Systems.

The striatum supports learning from immediate feedback by coding prediction errors (PEs), whereas the hippocampus (HC) plays a parallel role in learning from delayed feedback. Both regions show evidence of decline in human aging, but behavioral research suggests greater decline in HC versus striatal functions. The present study included male and female humans and used fMRI to examine younger and older adults' brain activation patterns during a learning task with choice feedback presented immediately or after a brief delay. Participants then completed a surprise memory task that tested their recognition of trial-unique feedback stimuli, followed by assessments of postlearning cue preference, outcome probability awareness, and willingness to pay. The study yielded three main findings. First, behavioral measures indicated similar rates of learning in younger and older adults across conditions, but postlearning measures indicated impairment in older adults' ability to subsequently apply learning to discriminate between cues. Second, PE signals in the striatum were greater for immediate versus delayed feedback in both age groups, but PE signals in the HC were greater for delayed versus immediate feedback only in younger adults. Third, unlike younger adults, older adults failed to exhibit enhanced episodic memory for outcome stimuli in the delayed-feedback condition. Together, these findings indicate that HC circuits supporting learning and memory decline more than striatal circuits in healthy aging, which suggests that declines in HC learning signals may be an important predictor of deficits in learning-dependent economic decisions among older adults.SIGNIFICANCE STATEMENT The hippocampus (HC) and striatum play distinct and critical roles in learning. Substantial research suggests that age-related decline in learning supported by the HC outpaces decline in learning supported by the striatum; however, such inferences have been drawn by comparing performance in tasks with fundamentally different structures. The present study overcomes this obstacle by implementing a single fMRI-learning paradigm with a subtle variation in feedback timing to examine differential age effects on memory supported by the HC and striatum. Our results provide converging behavioral and brain-imaging evidence showing that HC circuits supporting learning and memory decline more than striatal circuits in healthy aging and that declines in HC learning signals may predict early deficits in learning-dependent decisions among older adults.