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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., Competing Interests: The authors declare no competing financial interests., (Copyright © 2024 the authors.)

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., (Copyright © 2023 the authors.)

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., (Copyright © 2023 the authors.)

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., (Copyright © 2020 the authors.)

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., (Copyright © 2020 the authors.)

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., (Copyright © 2018 the authors 0270-6474/18/388453-10$15.00/0.)

Although it is known that brain regions in one hemisphere may interact very closely with their corresponding contralateral regions (collaboration) or operate relatively independent of them (segregation), the specific brain regions (where) and conditions (how) associated with collaboration or segregation are largely unknown. We investigated these issues using a split field-matching task in which participants matched the meaning of words or the visual features of faces presented to the same (unilateral) or to different (bilateral) visual fields. Matching difficulty was manipulated by varying the semantic similarity of words or the visual similarity of faces. We assessed the white matter using the fractional anisotropy (FA) measure provided by diffusion tensor imaging (DTI) and cross-hemispheric communication in terms of fMRI-based connectivity between homotopic pairs of cortical regions. For both perceptual and semantic matching, bilateral trials became faster than unilateral trials as difficulty increased (bilateral processing advantage, BPA). The study yielded three novel findings. First, whereas FA in anterior corpus callosum (genu) correlated with word-matching BPA, FA in posterior corpus callosum (splenium-occipital) correlated with face-matching BPA. Second, as matching difficulty intensified, cross-hemispheric functional connectivity (CFC) increased in domain-general frontopolar cortex (for both word and face matching) but decreased in domain-specific ventral temporal lobe regions (temporal pole for word matching and fusiform gyrus for face matching). Last, a mediation analysis linking DTI and fMRI data showed that CFC mediated the effect of callosal FA on BPA. These findings clarify the mechanisms by which the hemispheres interact to perform complex cognitive tasks., (Copyright © 2015 the authors 0270-6474/15/358191-10$15.00/0.)

Everyday consumer choices frequently involve memory, as when we retrieve information about consumer products when making purchasing decisions. In this context, poor memory may affect decision quality, particularly in individuals with memory decline, such as older adults. However, age differences in choice behavior may be reduced if older adults can recruit additional neural resources that support task performance. Although such functional compensation is well documented in other cognitive domains, it is presently unclear whether it can support memory-guided decision making and, if so, which brain regions play a role in compensation. The current study engaged younger and older humans in a memory-dependent choice task in which pairs of consumer products from a popular online-shopping site were evaluated with different delays between the first and second product. Using functional imaging (fMRI), we found that the ventromedial prefrontal cortex (vmPFC) supports compensation as defined by three a priori criteria: (1) increased vmPFC activation was observed in older versus younger adults; (2) age-related increases in vmPFC activity were associated with increased retrieval demands; and (3) increased vmPFC activity was positively associated with performance in older adults-evidence of successful compensation. Extending these results, we observed evidence for compensation in connectivity between vmPFC and the dorsolateral PFC during memory-dependent choice. In contrast, we found no evidence for age differences in value-related processing or age-related compensation for choices without delayed retrieval. Together, these results converge on the conclusion that age-related decline in memory-dependent choice performance can be minimized via functional compensation in vmPFC., (Copyright © 2014 the authors 0270-6474/14/3415648-10$15.00/0.)

Although it is well established that the perirhinal cortex (PRC) makes an important contribution to recognition memory, the specific nature of this contribution remains uncertain. The finding that PRC activity is reduced for old compared with new items is typically attributed to the recovery of a long-term memory (LTM) signal. However, because old items are processed more easily or fluently than new items, reduced PRC activity could reflect increased fluency rather than LTM retrieval per se. We tested this hypothesis in humans using fMRI and a well-validated method to manipulate fluency: the masked priming paradigm. Some words during an old-new recognition test were preceded by conceptually related words (primes) that were subliminally presented (masked). The behavioral results replicated previous findings using this paradigm, whereby the fluency manipulation increased "oldness" responses to both old and new items. The fMRI analyses yielded two main sets of results. First, in the case of new items, which are independent from LTM retrieval, masked priming reduced PRC activity and predicted behavioral misattribution of fluency to oldness. Second, in the case of old items, the same PRC region showing fluency-related reductions for new items also contributed to "old" responding to old items. Individual differences in PRC attenuation also predicted oldness ratings to old items, and fluency modulated PRC connectivity with other brain regions associated with processing oldness signals, including visual cortex and right lateral prefrontal cortex. These results support a broader view in which the PRC serves a function more general than memory.

The rivalry between the men's basketball teams of Duke University and the University of North Carolina-Chapel Hill (UNC) is one of the most storied traditions in college sports. A subculture of students at each university form social bonds with fellow fans, develop expertise in college basketball rules, team statistics, and individual players, and self-identify as a member of a fan group. The present study capitalized on the high personal investment of these fans and the strong affective tenor of a Duke-UNC basketball game to examine the neural correlates of emotional memory retrieval for a complex sporting event. Male fans watched a competitive, archived game in a social setting. During a subsequent functional magnetic resonance imaging session, participants viewed video clips depicting individual plays of the game that ended with the ball being released toward the basket. For each play, participants recalled whether or not the shot went into the basket. Hemodynamic signal changes time locked to correct memory decisions were analyzed as a function of emotional intensity and valence, according to the fan's perspective. Results showed intensity-modulated retrieval activity in midline cortical structures, sensorimotor cortex, the striatum, and the medial temporal lobe, including the amygdala. Positively valent memories specifically recruited processing in dorsal frontoparietal regions, and additional activity in the insula and medial temporal lobe for positively valent shots recalled with high confidence. This novel paradigm reveals how brain regions implicated in emotion, memory retrieval, visuomotor imagery, and social cognition contribute to the recollection of specific plays in the mind of a sports fan.

Does the parietal lobe have a critical role in memory? The neuroimaging literature indicates that it has an important role, especially in episodic memory. However, the neuropsychological literature suggests that its role is more limited to attentional, spatial, or imagery aspects of memory. Here, we present data to adjudicate this disagreement. Two patients with bilateral parietal lobe damage received detailed assessments of their autobiographical memories. The results show that although both patients easily recalled various memories, their freely recalled memories were relatively impoverished, lacking in detail. This deficit was ubiquitous, and not limited to spatial or perceptual aspects of memory. The memory deficit disappeared when memory was specifically probed by asking pointed questions. Additional tests show that it is unlikely that their free recall deficit can be explained by general mental imagery problems. In sum, the parietal lobe appears to have a critical role in recollection aspects of episodic memory.

Although memory confidence and accuracy tend to be positively correlated, people sometimes remember with high confidence events that never happened. How can confidence correlate with accuracy but apply also to illusory memories? One possible explanation is that high confidence in veridical versus illusory memories depends on different neural mechanisms. The present study investigated this possibility using functional magnetic resonance imaging and a modified version of the Deese-Roediger-McDermott false-memory paradigm. Participants read short lists of categorized words, and brain activity was measured while they performed a recognition test with confidence rating. The study yielded three main findings. First, compared with low-confidence responses, high-confidence responses were associated with medial temporal lobe (MTL) activity in the case of true recognition but with frontoparietal activity in the case of false recognition. Second, these regions showed significant confidence-by-veridicality interactions. Finally, only MTL regions showed greater activity for high-confidence true recognition than for high-confidence false recognition, and only frontoparietal regions showed greater activity for high-confidence false recognition than for high-confidence true recognition. These findings indicate that confidence in true recognition is mediated primarily by a recollection-related MTL mechanism, whereas confidence in false recognition reflects mainly a familiarity-related frontoparietal mechanism. This account is consistent with the fuzzy trace theory of false recognition. Correlation analyses revealed that MTL and frontoparietal regions play complementary roles during episodic retrieval. In sum, the present study shows that when one focuses exclusively on high-confidence responses, the neural correlates of true and false memory are clearly different.

Although it is widely accepted that the medial temporal lobes (MTLs) are critical for becoming aware that something happened in the past, there is virtually no evidence whether MTL sensitivity to event oldness also depends on conscious awareness. Using event-related functional magnetic resonance imaging, we show that activity in posterior MTL tracks whether an item is actually old (true oldness), regardless of participants' awareness of oldness (perceived oldness). Confirming its sensitivity to the objective nature of the stimulus, activity in this region was strongly correlated with individual memory performance (r = 0.74). At the same time, we found that memory errors (misses) were associated with activity in an anterior MTL region, which signaled whether an item was consciously experienced as new (perceived novelty). Logistic regression analyses based on individual trial activity indicated that the two MTL regions showed opposing relationships with behavior, and that memory performance was determined by their joint activity. Furthermore, functional connectivity analyses showed that perceived novelty activity in the ANTERIOR [corrected] MTL inhibited true oldness activity in the POSTERIOR [corrected] MTL. These findings indicate that participants' behavior reflected the combined effects of multiple MTL regions. More generally, our results show that parts of MTL can distinguish old from new independently of consciousness.

Using event-related functional magnetic resonance imaging, we identified brain regions involved in successful relational memory (RM) during encoding and retrieval for semantic and perceptual associations or in general, independent of phase and content. Participants were scanned while encoding and later retrieving associations between pairs of words (semantic RM) or associations between words and fonts (perceptual RM). Encoding success activity (ESA) was identified by comparing study-phase activity for items subsequently remembered (hits) versus forgotten (misses) and retrieval success activity (RSA) by comparing test-phase activity for hits versus misses. The study yielded three main sets of findings. First, ESA-RSA differences were found within the medial temporal lobes (MTLs) and within the prefrontal cortex (PFC). Within the left MTL, ESA was greater in the anterior hippocampus, and RSA was greater in the posterior parahippocampal cortex/hippocampus. This finding is consistent with the notion of an encoding-retrieval gradient along the longitudinal MTL axis. Within the left PFC, ESA was greater in ventrolateral PFC, and RSA was greater in dorsolateral and anterior PFC. This is the first evidence of a dissociation in successful encoding and retrieval activity within left PFC. Second, consistent with the transfer-appropriate processing principle, some ESA regions were reactivated during RSA in a content-specific manner. For semantic RM, these regions included the left ventrolateral PFC, whereas for perceptual RM, they included occipitoparietal and right parahippocampal regions. Finally, only one region in the entire brain was associated with RM in general (i.e., for both semantic and perceptual ESA and RSA): the left hippocampus. This finding highlights the fundamental role of the hippocampus in RM.

Positron emission tomography (PET) was used to compare regional cerebral blood flow (rCBF) in young (mean 26 years) and old (mean 70 years) subjects while they were encoding, recognizing, and recalling word pairs. A multivariate partial-least-squares (PLS) analysis of the data was used to identify age-related neural changes associated with (1) encoding versus retrieval and (2) recognition versus recall. Young subjects showed higher activation than old subjects (1) in left prefrontal and occipito-temporal regions during encoding and (2) in right prefrontal and parietal regions during retrieval. Old subjects showed relatively higher activation than young subjects in several regions, including insular regions during encoding, cuneus/precuneus regions during recognition, and left prefrontal regions during recall. Frontal activity in young subjects was left-lateralized during encoding and right-lateralized during recall [hemispheric encoding/retrieval asymmetry (HERA)], whereas old adults showed little frontal activity during encoding and a more bilateral pattern of frontal activation during retrieval. In young subjects, activation in recall was higher than that in recognition in cerebellar and cingulate regions, whereas recognition showed higher activity in right temporal and parietal regions. In old subjects, the differences in blood flow between recall and recognition were smaller in these regions, yet more pronounced in other regions. Taken together, the results indicate that advanced age is associated with neural changes in the brain systems underlying encoding, recognition, and recall. These changes take two forms: (1) age-related decreases in local regional activity, which may signal less efficient processing by the old, and (2) age-related increases in activity, which may signal functional compensation.

Two important objectives in the neuroscience of memory are (1) identification of neural pathways involved in memory processes; and (2) characterization of the pattern of interactions between these pathways. Functional neuroimaging can contribute to both of these goals. Using image subtraction analysis of regional cerebral blood flow data measured with positron emission tomography, we identified brain regions that changed activity during episodic memory retrieval (visual work recognition). Relative to a baseline reading task, decreased activity was observed in bilateral prefrontal, bilateral anterior and posterior temporal, and posterior cingulate cortices. Brain regions showing increased activity were the right prefrontal (different from deactivated regions), left anterior cingulate, and left occipital cortices, and vermis of cerebellum. We then performed a network analysis with structural equation modeling to test the hypothesis that regional decreases came about through active inhibition by regions showing increased activity during retrieval. This analysis demonstrated that the influence of activated regions on deactivated regions was more negative during retrieval than during reading, confirming the inhibition hypothesis. Such confirmation could not have been made from the subtraction analysis alone because decreases can come about, at the very least, through reduction of functional influences as well as by active inhibition. The concepts of ensemble excitation and inhibition, as defined through network analysis, are introduced. We argue that is is critical to examine the combined pattern of excitatory and inhibitory influences to fully appreciate the neural basis of episodic memory.