Spatial context scaffolds long-term episodic richness of weaker real-world autobiographical memories in both older and younger adults.

Remembering life experiences involves recalling not only what occurred (episodic details), but also where an event took place (spatial context), both of which decline with age. Although spatial context can cue episodic detail recollection, it is unknown whether initially recalling an event alongside greater reinstatement of spatial context protects memory for episodic details in the long term, and whether this is affected by age. Here, we analysed 1079 personally-experienced, real-world events from 29 older adults and 12 younger adults. Events were recalled first on average 6 weeks after they occurred and then again on average 24 weeks after they occurred. We developed a novel scoring protocol to quantify spatial contextual details and used the established Autobiographical Interview to quantify episodic details. We found improved recall of episodic details after a delay if those details had initially been recalled situated in greater spatial context. Notably, for both older and younger adults, this preservation was observed for memories initially recalled with low, but not high, numbers of episodic details, suggesting that spatial context aided episodic retrieval for memories that required more support. This work supports the notion that spatial context scaffolds detail-rich event recollection and inspires memory interventions that leverage this spatial scaffold.

Experience transforms crossmodal object representations in the anterior temporal lobes.

Combining information from multiple senses is essential to object recognition, core to the ability to learn concepts, make new inferences, and generalize across distinct entities. Yet how the mind combines sensory input into coherent crossmodal representations - the crossmodal binding problem - remains poorly understood. Here, we applied multi-echo fMRI across a 4-day paradigm, in which participants learned three-dimensional crossmodal representations created from well-characterized unimodal visual shape and sound features. Our novel paradigm decoupled the learned crossmodal object representations from their baseline unimodal shapes and sounds, thus allowing us to track the emergence of crossmodal object representations as they were learned by healthy adults. Critically, we found that two anterior temporal lobe structures - temporal pole and perirhinal cortex - differentiated learned from non-learned crossmodal objects, even when controlling for the unimodal features that composed those objects. These results provide evidence for integrated crossmodal object representations in the anterior temporal lobes that were different from the representations for the unimodal features. Furthermore, we found that perirhinal cortex representations were by default biased toward visual shape, but this initial visual bias was attenuated by crossmodal learning. Thus, crossmodal learning transformed perirhinal representations such that they were no longer predominantly grounded in the visual modality, which may be a mechanism by which object concepts gain their abstraction.

Involuntary memory signals in the medial temporal lobe.

We highlight recent progress in neuroimaging and neuropsychological research on memory mechanisms in the medial temporal lobe that speaks to the involuntary nature of memory retrieval processes. We suggest that evidence form these studies supports Barzykowski and Moulin's proposal that memory signals involved in experiences of familiarity and déjà vu can be generated in the absence of retrieval intentionality.

Perception and Memory in the Ventral Visual Stream and Medial Temporal Lobe.

Perception and memory are traditionally thought of as separate cognitive functions, supported by distinct brain regions. The canonical perspective is that perceptual processing of visual information is supported by the ventral visual stream, whereas long-term declarative memory is supported by the medial temporal lobe. However, this modular framework cannot account for the increasingly large body of evidence that reveals a role for early visual areas in long-term recognition memory and a role for medial temporal lobe structures in high-level perceptual processing. In this article, we review relevant research conducted in humans, nonhuman primates, and rodents. We conclude that the evidence is largely inconsistent with theoretical proposals that draw sharp functional boundaries between perceptual and memory systems in the brain. Instead, the weight of the empirical findings is best captured by a representational-hierarchical model that emphasizes differences in content, rather than in cognitive processes within the ventral visual stream and medial temporal lobe.

Resolving Cross-modal Semantic Interference among Object Concepts Requires Medial Temporal Lobe Cortex.

The ability to flexibly categorize object concepts is essential to semantic cognition because the features that make two objects similar in one context may be irrelevant and even constitute interference in another. Thus, adaptive behavior in complex and dynamic environments requires the resolution of feature-based interference. In the current case study, we placed visual and functional semantic features in opposition across object concepts in two categorization tasks. Successful performance required the resolution of functional interference in a visual categorization task and the resolution of visual interference in a functional categorization task. In Experiment 1, we found that patient D. A., an individual with bilateral temporal lobe lesions, was unable to categorize object concepts in a context-dependent manner. His impairment was characterized by an increased tendency to incorrectly group objects that were similar on the task-irrelevant dimension, revealing an inability to resolve cross-modal semantic interference. In Experiment 2, D. A.'s categorization accuracy was comparable to controls when lures were removed, indicating that his impairment is unique to contexts that involve cross-modal interference. In Experiment 3, he again performed as well as controls when categorizing simple concepts, suggesting that his impairment is specific to categorization of complex object concepts. These results advance our understanding of the anterior temporal lobe as a system that represents object concepts in a manner that enables flexible semantic cognition. Specifically, they reveal a dissociation between semantic representations that contribute to the resolution of cross-modal interference and those that contribute to the resolution of interference within a given modality.

A smartphone intervention that enhances real-world memory and promotes differentiation of hippocampal activity in older adults.

The act of remembering an everyday experience influences how we interpret the world, how we think about the future, and how we perceive ourselves. It also enhances long-term retention of the recalled content, increasing the likelihood that it will be recalled again. Unfortunately, the ability to recollect event-specific details and reexperience the past tends to decline with age. This decline in recollection may reflect a corresponding decrease in the distinctiveness of hippocampal memory representations. Despite these well-established changes, there are few effective cognitive behavioral interventions that target real-world episodic memory. We addressed this gap by developing a smartphone-based application called HippoCamera that allows participants to record labeled videos of everyday events and subsequently replay, high-fidelity autobiographical memory cues. In two experiments, we found that older adults were able to easily integrate this noninvasive intervention into their daily lives. Using HippoCamera to repeatedly reactivate memories for real-world events improved episodic recollection and it evoked more positive autobiographical sentiment at the time of retrieval. In both experiments, these benefits were observed shortly after the intervention and again after a 3-mo delay. Moreover, more detailed recollection was associated with more differentiated memory signals in the hippocampus. Thus, using this smartphone application to systematically reactivate memories for recent real-world experiences can help to maintain a bridge between the present and past in older adults.

Activity in perirhinal and entorhinal cortex predicts perceived visual similarities among category exemplars with highest precision.

Vision neuroscience has made great strides in understanding the hierarchical organization of object representations along the ventral visual stream (VVS). How VVS representations capture fine-grained visual similarities between objects that observers subjectively perceive has received limited examination so far. In the current study, we addressed this question by focussing on perceived visual similarities among subordinate exemplars of real-world categories. We hypothesized that these perceived similarities are reflected with highest fidelity in neural activity patterns downstream from inferotemporal regions, namely in perirhinal (PrC) and anterolateral entorhinal cortex (alErC) in the medial temporal lobe. To address this issue with functional magnetic resonance imaging (fMRI), we administered a modified 1-back task that required discrimination between category exemplars as well as categorization. Further, we obtained observer-specific ratings of perceived visual similarities, which predicted behavioural discrimination performance during scanning. As anticipated, we found that activity patterns in PrC and alErC predicted the structure of perceived visual similarity relationships among category exemplars, including its observer-specific component, with higher precision than any other VVS region. Our findings provide new evidence that subjective aspects of object perception that rely on fine-grained visual differentiation are reflected with highest fidelity in the medial temporal lobe.

Neuroscience: Connecting the dots in memory.

The hippocampus supports the encoding and retrieval of event memories, but it is unclear how it organizes this information to facilitate efficient retrieval. A recent study suggests that it does so by integrating events based on their narrative structure.

Relationship between déjà vu experiences and recognition-memory impairments in temporal-lobe epilepsy.

Déjà vu is characterised by feelings of familiarity and concurrent awareness that this familiarity is wrong. Previous neuropsychological research has linked déjà vu during seizures in individuals with unilateral temporal-lobe epilepsy (uTLE) to rhinal-cortex abnormalities, and to recognition-memory deficits that selectively affect familiarity assessment. Here, we examined whether bilateral TLE patients with déjà vu (bTLE) show a similar pattern of performance. Using two experimental tasks, we found that bTLE patients exhibit deficits not only for familiarity but also for recollection. Relative to uTLE, this broader impairment also involved hippocampal abnormalities. Our findings confirm rhinal-cortex contributions to the generation of false familiarity in déjà vu that parallel its contributions to familiarity on recognition-memory tasks. While they do not rule out a role for recollection in identifying this familiarity as wrong, the deficits observed in bTLE patients weigh against the notion that any such role is necessary for déjà vu to occur.

Familiarity impairments after anterior temporal-lobe resection with hippocampal sparing: Lessons learned from case NB.

We review evidence from an extensive single case study in an individual (NB) who underwent a rare left-sided anterior temporal-lobe resection with sparing of the hippocampus. Our study aimed to determine whether memory functions of perirhinal cortex, which was largely removed in the resection, can be impaired against a background of preserved hippocampus-dependent memory processing. This research was guided by the proposal that item-based familiarity assessment relies on contributions of perirhinal cortex, and that the hippocampus plays a unique role in the relational binding of items to episodic contexts, which is critical for recollection. Seven sets of findings have emerged from our research on NB (synthesized from five primary research articles), and from follow-up work in other patients: (i) Familiarity impairments can be selective and be revealed with multiple methods; (ii) selective familiarity and selective recollection impairments can be double dissociated; (iii) selective familiarity impairments show material specificity; (iv) selective familiarity impairments extend to assessment of cumulative lifetime experience; (v) selective familiarity impairments are sensitive to degree of feature overlap between object concepts; (vi) selective familiarity impairments are associated with preserved task-related fMRI signals in the hippocampus; (vii) selective familiarity impairments can be observed in other lesion cases. Despite our main focus on the dual-process framework, we also discuss implications for the functional organization of the medial temporal lobes in broader terms. We argue that our findings shed light on this organization even if the functional specialization of different medial temporal structures is ultimately not fully captured with reference to the cognitive distinction between familiarity and recollection.

When Gist and Familiarity Collide: Evidence From False Recognition in Younger and Older Adults.

OBJECTIVES: Aging is associated with decreased recollection required to offset misleading effects of familiarity, as well as an increased mnemonic reliance on gist-based over detail-based information. We tested the novel hypothesis that age-related decrements in overriding familiarity can be eliminated under conditions in which gist-based information facilitates retrieval. METHOD: Twenty-seven younger adults and 27 older adults viewed scenes from two categories in an incidental encoding phase. In a recognition phase, old scenes were intermixed with new scenes from the studied categories and an unstudied category, with each new scene reappearing after 4, 18, or 48 intervening scenes. Participants were to respond "yes" to old scenes, and "no" to new scenes, including their repetitions. RESULTS: Despite encoding the scenes similarly, older adults made more false endorsements of new and repeated new scenes from studied categories. Both groups, however, were equally unlikely to falsely recognize new and repeated new scenes from the unstudied category. DISCUSSION: When helpful gist and misleading familiarity collide, gist wins, and eliminates age-related increases in false recognition.

Understanding perirhinal contributions to perception and memory: Evidence through the lens of selective perirhinal damage.

Although a memory systems view of the medial temporal lobe (MTL) has been widely influential in understanding how memory processes are implemented, a large body of work across humans and animals has converged on the idea that the MTL can support various other decisions, beyond those involving memory. Specifically, recent work suggests that perception of and memory for visual representations may interact in order to support ongoing cognition. However, given considerations involving lesion profiles in neuropsychological investigations and the correlational nature of fMRI, the precise nature of representations supported by the MTL are not well understood in humans. In the present investigation, three patients with highly specific lesions to MTL were administered a task that taxed perceptual and mnemonic judgments with highly similar face stimuli. A striking double dissociation was observed such that I.R., a patient with a cyst localized to right posterior PRc, displayed a significant impairment in perceptual discriminations, whereas patient A.N., an individual with a lesion in right posterior parahippocampal cortex and the tail of the right hippocampus, and S.D., an individual with bilateral hippocampal damage, did not display impaired performance on the perceptual task. A.N. and S.D. did, however, show impairments in memory performance, whereas patient I.R. did not. These results causally implicate right PRc in successful perceptual oddity judgments, however they suggest that representations supported by PRc are not necessary for correct mnemonic judgments, even in situations of high featural overlap.

Animacy and real-world size shape object representations in the human medial temporal lobes.

Identifying what an object is, and whether an object has been encountered before, is a crucial aspect of human behavior. Despite this importance, we do not yet have a complete understanding of the neural basis of these abilities. Investigations into the neural organization of human object representations have revealed category specific organization in the ventral visual stream in perceptual tasks. Interestingly, these categories fall within broader domains of organization, with reported distinctions between animate, inanimate large, and inanimate small objects. While there is some evidence for category specific effects in the medial temporal lobe (MTL), in particular in perirhinal and parahippocampal cortex, it is currently unclear whether domain level organization is also present across these structures. To this end, we used fMRI with a continuous recognition memory task. Stimuli were images of objects from several different categories, which were either animate or inanimate, or large or small within the inanimate domain. We employed representational similarity analysis (RSA) to test the hypothesis that object-evoked responses in MTL structures during recognition-memory judgments also show evidence for domain-level organization along both dimensions. Our data support this hypothesis. Specifically, object representations were shaped by either animacy, real-world size, or both, in perirhinal and parahippocampal cortex, and the hippocampus. While sensitivity to these dimensions differed across structures when probed individually, hinting at interesting links to functional differentiation, similarities in organization across MTL structures were more prominent overall. These results argue for continuity in the organization of object representations in the ventral visual stream and the MTL.

Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream.

A significant body of research in cognitive neuroscience is aimed at understanding how object concepts are represented in the human brain. However, it remains unknown whether and where the visual and abstract conceptual features that define an object concept are integrated. We addressed this issue by comparing the neural pattern similarities among object-evoked fMRI responses with behavior-based models that independently captured the visual and conceptual similarities among these stimuli. Our results revealed evidence for distinctive coding of visual features in lateral occipital cortex, and conceptual features in the temporal pole and parahippocampal cortex. By contrast, we found evidence for integrative coding of visual and conceptual object features in perirhinal cortex. The neuroanatomical specificity of this effect was highlighted by results from a searchlight analysis. Taken together, our findings suggest that perirhinal cortex uniquely supports the representation of fully specified object concepts through the integration of their visual and conceptual features.

How landmark suitability shapes recognition memory signals for objects in the medial temporal lobes.

A role of perirhinal cortex (PrC) in recognition memory for objects has been well established. Contributions of parahippocampal cortex (PhC) to this function, while documented, remain less well understood. Here, we used fMRI to examine whether the organization of item-based recognition memory signals across these two structures is shaped by object category, independent of any difference in representing episodic context. Guided by research suggesting that PhC plays a critical role in processing landmarks, we focused on three categories of objects that differ from each other in their landmark suitability as confirmed with behavioral ratings (buildings > trees > aircraft). Participants made item-based recognition-memory decisions for novel and previously studied objects from these categories, which were matched in accuracy. Multi-voxel pattern classification revealed category-specific item-recognition memory signals along the long axis of PrC and PhC, with no sharp functional boundaries between these structures. Memory signals for buildings were observed in the mid to posterior extent of PhC, signals for trees in anterior to posterior segments of PhC, and signals for aircraft in mid to posterior aspects of PrC and the anterior extent of PhC. Notably, item-based memory signals for the category with highest landmark suitability ratings were observed only in those posterior segments of PhC that also allowed for classification of landmark suitability of objects when memory status was held constant. These findings provide new evidence in support of the notion that item-based memory signals for objects are not limited to PrC, and that the organization of these signals along the longitudinal axis that crosses PrC and PhC can be captured with reference to landmark suitability.

Familiarity and recollection vs representational models of medial temporal lobe structures: A single-case study.

Although it is known that medial temporal lobe (MTL) structures support declarative memory, the fact these structures have different architectonics and circuitry suggests they may also play different functional roles. Selective lesions of MTL structures offer an opportunity to understand these roles. We report, in this study, on JMG, a patient who presents highly unusual lesions that completely affected all MTL structures except for the right hippocampus and parts of neighbouring medial parahippocampal cortex. We first demonstrate that JMG shows preserved recall for visual material on 5 experimental tasks. This finding suggests that his right hippocampus is functional, even though it appears largely disconnected from most of its MTL afferents. In contrast, JMG performed very poorly, as compared to control subjects, on 7 tasks of visual recognition memory for single items. Although he sometimes performed above chance, neither familiarity nor recollection appeared fully preserved. These results indicate that extrahippocampal structures, damaged bilaterally in JMG, perform critical operations for item recognition; and that the hippocampus cannot take over that role, including recollection, when these structures are largely damaged. Finally, in a set of 3 recognition memory tasks with scenes as stimuli, JMG performed at the level of control participants and obtained normal indices of familiarity and recollection. Overall, our findings suggest that the right hippocampus and remnants of parahippocampal cortex can support recognition memory for scenes in the absence of preserved item-recognition memory. The patterns of dissociations, which we report in the present study, provide support for a representational account of the functional organization of MTL structures.

Perirhinal cortex tracks degree of recent as well as cumulative lifetime experience with object concepts.

Evidence from numerous sources indicates that recognition of the prior occurrence of objects requires computations of perirhinal cortex (PrC) in the medial temporal lobe (MTL). Extant research has primarily probed recognition memory based on item exposure in a recent experimental study episode. Outside the laboratory, however, familiarity for objects typically accrues gradually with learning across many different episodic contexts, which can be distributed over a lifetime of experience. It is currently unknown whether PrC also tracks this cumulative lifetime experience with object concepts. To address this issue, we conducted a functional magnetic resonance imaging (fMRI) experiment in healthy individuals in which we compared judgments of the perceived lifetime familiarity with object concepts, a task that has previously been employed in many normative studies on concept knowledge, with frequency judgments for recent laboratory exposure in a study phase. Guided by neurophysiological data showing that neurons in primate PrC signal prior object exposure at multiple time scales, we predicted that PrC responses would track perceived prior experience in both types of judgments. Left PrC and a number of cortical regions that are often co-activated as part of the default-mode network showed an increase in Blood-Oxygen-Level Dependent (BOLD) response in relation to increases in the perceived cumulative lifetime familiarity of object concepts. These regions included the left hippocampus, left mid-lateral temporal cortex, as well as anterior and posterior cortical midline structures. Critically, left PrC was found to be the only region that showed this response in combination with the typically observed decrease in signal for perceived recent exposure in the experimental study phase. These findings provide, to our knowledge, the first evidence that ties signals in human PrC to variations in cumulative lifetime experience with object concepts. They offer a new link between the role of PrC in recognition memory and its broader role in conceptual processing.

Distributed category-specific recognition-memory signals in human perirhinal cortex.

Evidence from a large body of research suggests that perirhinal cortex (PrC), which interfaces the medial temporal lobe with the ventral visual pathway for object identification, plays a critical role in item-based recognition memory. The precise manner in which PrC codes for the prior occurrence of objects, however, remains poorly understood. In the present functional magnetic resonance imaging (fMRI) study, we used multivoxel pattern analyses to examine whether the prior occurrence of faces is coded by distributed patterns of PrC activity that consist of voxels with decreases as well as increases in signal. We also investigated whether pertinent voxels are preferentially tuned to the specific object category to which judged stimuli belong. We found that, when no a priori constraints were imposed on the direction of signal change, activity patterns that allowed for successful classification of recognition-memory decisions included some voxels with decreases and others with increases in signal in association with perceived prior occurrence. Moreover, successful classification was obtained in the absence of a mean difference in activity across the set of voxels in these patterns. Critically, we observed a positive relationship between classifier accuracy and behavioral performance across participants. Additional analyses revealed that voxels carrying diagnostic information for classification of memory decisions showed category specificity in their tuning for faces when probed with an independent functional localizer in a nonmnemonic task context. These voxels were spatially distributed in PrC, and extended beyond the contiguous voxel clusters previously described as the anterior temporal face patch. Our findings provide support for proposals, recently raised in the neurophysiological literature, that the prior occurrence of objects is coded by distributed PrC representations. They also suggest that the stimulus category to which an item belongs shapes the organization of these distributed representations.

Distinct familiarity-based response patterns for faces and buildings in perirhinal and parahippocampal cortex.

An unresolved question in our understanding of the medial temporal lobes is how functional differences between structures pertaining to stimulus category relate to the distinction between item-based and contextually based recognition-memory processes. Specifically, it remains unclear whether perirhinal cortex (PrC) supports item-based familiarity signals for all stimulus categories or whether parahippocampal cortex (PhC) may also play a role for stimulus categories that are known to engage this structure in other task contexts. Here, we used multivoxel pattern analyses of fMRI data to compare patterns of activity in humans that are associated with the perceived familiarity of faces, buildings, and chairs. During scanning, participants judged the familiarity of previously studied and novel items from all three categories. Instances in which recognition was based on recollection were removed from all analyses. In right PrC, we found patterns of activity that distinguished familiar from novel faces. By contrast, in right PhC, we observed such patterns for buildings. Familiarity signals for chairs were present in both structures but shared little overlap with the patterns observed for faces and buildings on a more fine-grained scale. In the hippocampus, we found no evidence for familiarity signals for any object category. Our findings show that both PrC and PhC contribute to the assessment of item familiarity. They suggest that PhC does not only represent episodic context but can also represent item information for some object categories in recognition-memory decisions. In turn, our findings also indicate that the involvement of PrC in representing item familiarity is not ubiquitous.