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.

Impaired perceptual discrimination of complex objects in older adults at risk for dementia.

Tau pathology accumulates in the perirhinal cortex (PRC) of the medial temporal lobe (MTL) during the earliest stages of the Alzheimer's disease (AD), appearing decades before clinical diagnosis. Here, we leveraged perceptual discrimination tasks that target PRC function to detect subtle cognitive impairment even in nominally healthy older adults. Older adults who did not have a clinical diagnosis or subjective memory complaints were categorized into "at-risk" (score <26; n = 15) and "healthy" (score ≥26; n = 23) groups based on their performance on the Montreal Cognitive Assessment. The task included two conditions known to recruit the PRC: faces and complex objects (greebles). A scene condition, known to recruit the hippocampus, and a size control condition that does not rely on the MTL were also included. Individuals in the at-risk group were less accurate than those in the healthy group for discriminating greebles. Performance on either the face or size control condition did not predict group status above and beyond that of the greeble condition. Visual discrimination tasks that are sensitive to PRC function may detect early cognitive decline associated with AD.

Sleep Differentially and Profoundly Impairs Recall Memory in a Patient with Fornix Damage.

In March 2020, C.T., a kind, bright, and friendly young woman underwent surgery for a midline tumor involving her septum pellucidum and extending down into her fornices bilaterally. Following tumor diagnosis and surgery, C.T. experienced significant memory deficits: C.T.'s family reported that she could remember things throughout the day, but when she woke up in the morning or following a nap, she would expect to be in the hospital, forgetting all the information that she had learned before sleep. The current study aimed to empirically validate C.T.'s pattern of memory loss and explore its neurological underpinnings. On two successive days, C.T. and age-matched controls watched an episode of a TV show and took a nap or stayed awake before completing a memory test. Although C.T. performed numerically worse than controls in both conditions, sleep profoundly exacerbated her memory impairment, such that she could not recall any details following a nap. This effect was replicated in a second testing session. High-resolution MRI scans showed evidence of the trans-callosal surgical approach's impact on the mid-anterior corpus callosum, indicated that C.T. had perturbed white matter particularly in the right fornix column, and demonstrated that C.T.'s hippocampal volumes did not differ from controls. These findings suggest that the fornix is important for processing episodic memories during sleep. As a key output pathway of the hippocampus, the fornix may ensure that specific memories are replayed during sleep, maintain the balance of sleep stages, or allow for the retrieval of memories following sleep.

Recollection and prior knowledge recruit the left angular gyrus during recognition.

The human angular gyrus (AG) is implicated in recollection, or the ability to retrieve detailed memory content from a specific episode. A separate line of research examining the neural bases of more general mnemonic representations, extracted over multiple episodes, also highlights the AG as a core region of interest. To reconcile these separate views of AG function, the present fMRI experiment used a Remember-Know paradigm with famous (prior knowledge) and non-famous (no prior knowledge) faces to test whether AG activity could be modulated by both task-specific recollection and general prior knowledge within the same individuals. Increased BOLD activity in the left AG was observed during both recollection in the absence of prior knowledge (recollected > non-recollected or correctly rejected non-famous faces) and when prior knowledge was accessed in the absence of experiment-specific recollection (famous > non-famous correct rejections). This pattern was most prominent for the left AG as compared to the broader inferior parietal lobe. Recollection-related responses in the left AG increased with encoding duration and prior knowledge, despite prior knowledge being incidental to the recognition decision. Overall, the left AG appears sensitive to both task-specific recollection and the incidental access of general prior knowledge, thus broadening our notions of the kinds of mnemonic representations that drive activity in this region.

Unrestricted eye movements strengthen effective connectivity from hippocampal to oculomotor regions during scene construction.

Scene construction is a key component of memory recall, navigation, and future imagining, and relies on the medial temporal lobes (MTL). A parallel body of work suggests that eye movements may enable the imagination and construction of scenes, even in the absence of external visual input. There are vast structural and functional connections between regions of the MTL and those of the oculomotor system. However, the directionality of connections between the MTL and oculomotor control regions, and how it relates to scene construction, has not been studied directly in human neuroimaging. In the current study, we used dynamic causal modeling (DCM) to interrogate effective connectivity between the MTL and oculomotor regions using a scene construction task in which participants' eye movements were either restricted (fixed-viewing) or unrestricted (free-viewing). By omitting external visual input, and by contrasting free- versus fixed- viewing, the directionality of neural connectivity during scene construction could be determined. As opposed to when eye movements were restricted, allowing free-viewing during construction of scenes strengthened top-down connections from the MTL to the frontal eye fields, and to lower-level cortical visual processing regions, suppressed bottom-up connections along the visual stream, and enhanced vividness of the constructed scenes. Taken together, these findings provide novel, non-invasive evidence for the underlying, directional, connectivity between the MTL memory system and oculomotor system associated with constructing vivid mental representations of scenes.

The Influence of Cerebrovascular Pathology on Cluster Analysis of Neuropsychological Scores in Patients With Mild Cognitive Impairment.

OBJECTIVES: The diagnostic entity of mild cognitive impairment (MCI) is heterogeneous, highlighting the need for data-driven classification approaches to identify patient subgroups. However, these approaches can be strongly determined by sample characteristics and selected measures. Here, we applied a cluster analysis to an MCI patient database from a neuropsychology clinic to determine whether the inclusion of patients with MCI with vascular pathology would result in a different classification of subgroups. METHODS: Participants diagnosed with MCI (n = 166), vascular cognitive impairment-no dementia (n = 26), and a group of older adults with subjective cognitive concerns but no objective impairment (n = 144) were assessed using a full neuropsychological battery and other clinical measures. Cognitive measures were analyzed using a hierarchical cluster analysis and then a k-means approach, with resulting clusters compared on a range of demographic and clinical variables. RESULTS: We found a 4-factor solution: a cognitively intact cluster, a globally impaired cluster, an amnestic/visuospatial impairment cluster, and a mild, mixed-domain cluster. Interestingly, group differences in self-reported multilingualism emerged in the derived clusters that were not observed when comparing diagnostic groups. CONCLUSIONS: Our results were generally consistent with previous studies using cluster analysis in MCI. Including patients with primarily cerebrovascular disease resulted in subtle differences in the derived clusters and revealed new insights into shared cognitive profiles of patients beyond diagnostic categories. These profiles should be further explored to develop individualized assessment and treatment approaches.

Flexible Use of Spatial Frames of Reference for Object-Location Memory in Older Adults.

In memory, representations of spatial features are stored in different reference frames; features relative to our position are stored egocentrically and features relative to each other are stored allocentrically. Accessing these representations engages many cognitive and neural resources, and so is susceptible to age-related breakdown. Yet, recent findings on the heterogeneity of cognitive function and spatial ability in healthy older adults suggest that aging may not uniformly impact the flexible use of spatial representations. These factors have yet to be explored in a precisely controlled task that explicitly manipulates spatial frames of reference across learning and retrieval. We used a lab-based virtual reality task to investigate the relationship between object-location memory across frames of reference, cognitive status, and self-reported spatial ability. Memory error was measured using Euclidean distance from studied object locations to participants' responses at testing. Older adults recalled object locations less accurately when they switched between frames of reference from learning to testing, compared with when they remained in the same frame of reference. They also showed an allocentric learning advantage, producing less error when switching from an allocentric to an egocentric frame of reference, compared with the reverse direction of switching. Higher MoCA scores and better self-assessed spatial ability predicted less memory error, especially when learning occurred egocentrically. We suggest that egocentric learning deficits are driven by difficulty in binding multiple viewpoints into a coherent representation. Finally, we highlight the heterogeneity of spatial memory performance in healthy older adults as a potential cognitive marker for neurodegeneration, beyond normal aging.

Reframing spatial frames of reference: What can aging tell us about egocentric and allocentric navigation?

Representations of space in mind are crucial for navigation, facilitating processes such as remembering landmark locations, understanding spatial relationships between objects, and integrating routes. A significant problem, however, is the lack of consensus on how these representations are encoded and stored in memory. Specifically, the nature of egocentric and allocentric frames of reference in human memory is widely debated. Yet, in recent investigations of the spatial domain across the lifespan, these distinctions in mnemonic spatial frames of reference have identified age-related impairments. In this review, we survey the ways in which different terms related to spatial representations in memory have been operationalized in past aging research and suggest a taxonomy to provide a common language for future investigations and theoretical discussion. This article is categorized under: Psychology > Memory Neuroscience > Cognition Psychology > Development and Aging.