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Navigation is instrumental to daily life and is often used to encode and locate objects, such as keys in one's house. Yet, little is known about how navigation works in more ecologically valid situations such as finding objects within a room. Specifically, it is not clear how vision vs. body movements contribute differentially to spatial memory in such small-scale spaces. In the current study, participants encoded object locations by viewing them while standing (stationary condition) or by additionally being guided by the experimenter while blindfolded (walking condition) after viewing the objects. They then retrieved the objects from the same or different viewpoint, creating a 2 × 2 within subject design. We simultaneously recorded participant eye movements throughout the experiment using mobile eye tracking. The results showed no statistically significant differences among our four conditions (stationary, same viewpoint as encoding; stationary, different viewpoint; walking, same viewpoint; walking, different viewpoint), suggesting that in a small real-world space, vision may be sufficient to remember object locations. Eye tracking analyses revealed that object locations were better remembered next to landmarks and that participants encoded items on one wall together, suggesting the use of local wall coordinates rather than global room coordinates. A multivariate regression analysis revealed that the only significant predictor of object placement accuracy was average looking time. These results suggest that vision may be sufficient for encoding object locations in a small-scale environment and that such memories may be formed largely locally rather than globally. • Mobile eye tracking to characterize eye movements during naturalistic navigation. • Movement and viewpoint conditions did not affect placement error at retrieval. • Items next to landmarks were remembered better than items farther from landmarks. • Objects were encoded locally on each wall rather than globally using the whole room. • Longer average encoding durations of fixation to items predicted better memory. [ABSTRACT FROM AUTHOR]

Summary Low-frequency (delta/theta band) hippocampal neural oscillations play prominent roles in computational models of spatial navigation, but their exact function remains unknown. Some theories propose they are primarily generated in response to sensorimotor processing, while others suggest a role in memory-related processing. We directly recorded hippocampal EEG activity in patients undergoing seizure monitoring while they explored a virtual environment containing teleporters. Critically, this manipulation allowed patients to experience movement through space in the absence of visual and self-motion cues. The prevalence and duration of low-frequency hippocampal oscillations were unchanged by this manipulation, indicating that sensorimotor processing was not required to elicit them during navigation. Furthermore, the frequency-wise pattern of oscillation prevalence during teleportation contained spatial information capable of classifying the distance teleported. These results demonstrate that movement-related sensory information is not required to drive spatially informative low-frequency hippocampal oscillations during navigation and suggest a specific function in memory-related spatial updating. [ABSTRACT FROM AUTHOR]

Traumatic brain injury (TBI) often results in persistent attention and memory deficits that are associated with hippocampal dysfunction. Although deep brain stimulation (DBS) is used to treat neurological disorders related to motor dysfunction, the effectiveness of stimulation to treat cognition remains largely unknown. In this study, adult male Harlan Sprague-Dawley rats underwent a lateral fluid percussion or sham injury followed by implantation of bipolar electrodes in the medial septal nucleus (MSN) and ipsilateral hippocampus. In the first week after injury, there was a significant decrease in hippocampal theta oscillations that correlated with decreased object exploration and impaired performance in the Barnes maze spatial learning task. Continuous 7.7 Hz theta stimulation of the medial septum significantly increased hippocampal theta oscillations, restored normal object exploration, and improved spatial learning in injured animals. There were no benefits with 100 Hz gamma stimulation, and stimulation of sham animals at either frequency did not enhance performance. We conclude, therefore, that there was a theta frequency-specific benefit of DBS that restored cognitive function in brain-injured rats. These data suggest that septal theta stimulation may be an effective and novel neuromodulatory therapy for treatment of persistent cognitive deficits following TBI. [ABSTRACT FROM AUTHOR]

The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of "place cell" firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories. [ABSTRACT FROM AUTHOR]

Examining the function of individual human hippocampal subfields remains challenging because of their small sizes and convoluted structures. Previous human fMRI studies at 3 T have successfully detected differences in activation between hippocampal cornu ammonis (CA) field CA1, combined CA2, CA3, and dentate gyrus (DG) region (CA23DG), and the subiculum during associative memory tasks. In this study, we investigated hippocampal subfield activity in healthy participants using an associative memory paradigm during high-resolution fMRI scanning at 7 T. We were able to localize fMRI activity to anterior CA2 and CA3 during learning and to the posterior CA2 field, the CA1, and the posterior subiculum during retrieval of novel associations. These results provide insight into more specific human hippocampal subfield functions underlying learning and memory and a unique opportunity for future investigations of hippocampal subfield function in healthy individuals as well as those suffering from neurodegenerative diseases. [ABSTRACT FROM AUTHOR]

Spatial navigation and event memory (termed episodic memory) are thought to be heavily intertwined, both in terms of their cognitive processes and underlying neural systems. Some theoretical models posit that both memory for places during navigation and episodic memory depend on highly overlapping brain systems. Here, we assessed this relationship by testing navigation in an individual with severe retrograde and anterograde amnesia; the amnesia stemmed from bilateral lesions in the medial temporal lobes from two separate strokes. The individual with amnesia and age-matched controls were tested on their memories for the locations of previously seen objects relative to distal mountain cues in an immersive virtual environment involving free ambulation. All participants were tested from both repeated and novel start locations and when a single distal mountain cue was unknowingly moved to determine if they relied on a single (beacon) cue to a greater extent than the collection of all distal cues. Compared to age-matched controls, the individual with amnesia showed no significant deficits in navigation from either the repeated or novel start points, although both the individual with amnesia and controls performed well above chance at placing objects near their correct locations. The individual with amnesia also relied on a combination of distal cues in a manner comparable to age-matched controls. Despite largely intact memory for locations using distal cues, the individual with amnesia walked longer paths, rotated more, and took longer to complete trials. Our findings suggest that memory for places during navigation and episodic memory may involve partially dissociable brain circuits and that other brain regions outside of the medial temporal lobe partially support some aspects of navigation. At the same time, the fact that the individual with amnesia walked more circuitous paths and had dense amnesia for autobiographic events supports the idea that the hippocampus may be important for binding information as part of a larger role in memory. • We tested a person with severely impaired episodic memory on a spatial task with free ambulation and hidden target objects. • This individual had a bilateral lesion to the medial temporal lobes due to two separate strokes. • The individual performed comparably to controls and above chance at finding the hidden targets using distal cues. • Our findings support episodic and place memory involving partially dissociable brain circuits during navigation. [ABSTRACT FROM AUTHOR]

The rapid recognition and memory of faces and scenes implies the engagement of category-specific computational hubs in the ventral visual stream with the distributed cortical memory network. To better understand how recognition and identification occur in humans, we performed direct intracranial recordings, in a large cohort of patients (n = 50), from the medial parietal cortex (MPC) and the medial temporal lobe (MTL), structures known to be engaged during face and scene identification. We discovered that the MPC is topologically tuned to face and scene recognition, with clusters in MPC performing scene recognition bilaterally and face recognition in right subparietal sulcus. The MTL displayed a selectivity gradient with anterior, entorhinal cortex showing face selectivity and posterior parahippocampal regions showing scene selectivity. In both MPC and MTL, stimulus-specific identifiable exemplars led to greater activity in these cortical patches. These two regions work in concert for recognition of faces and scenes. Feature selectivity and identity-sensitive activity in the two regions was coincident, and they exhibited theta-phase locking during face and scene recognition. These findings together provide clear evidence for a specific role of subregions in the MPC for the recognition of unique entities. • Medial parietal cortex (MPC) has category-selective regions for faces and scenes • MPC subregions prefer recognizable examples of their selective stimuli • MPC shows category-selective interactions with medial temporal lobe (MTL) • MPC and MTL show coincident activity for category-specific identification Ventral visual and memory regions contain face- and scene-specific clusters of cortex. Woolnough et al. use multiregional intracranial recordings in a large cohort to reveal this organization extends to medial parietal cortex, which plays a role in our ability to identify faces and scenes, which it does via its connections with other memory regions. [ABSTRACT FROM AUTHOR]

Prior studies examining the neural mechanisms underlying retrieval success and precision have yielded inconsistent results. Here, the neural correlates of success and precision were examined with a memory task that assessed precision for spatial location. A sample of healthy young adults underwent functional magnetic resonance imaging scanning during a single study-test cycle. At study, participants viewed a series of object images, each placed at a randomly selected location on an imaginary circle. At test, studied images were intermixed with new images and presented to the participants. The requirement was to move a cursor to the location of the studied image, guessing if necessary. Participants then signaled whether the presented image had been studied. Memory precision was quantified as the angular difference between the studied location and the location selected by the participant. A precision effect was evident in the left angular gyrus, where BOLD activity covaried with location accuracy. In addition, multivoxel pattern analysis revealed a significant item-level reinstatement effect in the angular gyrus for high-precision trials. There was no evidence of a retrieval success effect in this region. BOLD activity in the hippocampus was insensitive to both success and precision. These findings are partially consistent with prior evidence that success and precision are dissociable features of memory retrieval., (© 2024 Massachusetts Institute of Technology.)

Prior studies examining the neural mechanisms underlying retrieval success and precision have yielded inconsistent results. Here, their neural correlates were examined using a memory task that assessed precision for spatial location. A sample of healthy young adults underwent fMRI scanning during a single study-test cycle. At study, participants viewed a series of object images, each placed at a randomly selected location on an imaginary circle. At test, studied images were intermixed with new images and presented to the participants. The requirement was to move a cursor to the location of the studied image, guessing if necessary. Participants then signaled whether the presented image as having been studied. Memory precision was quantified as the angle between the studied location and the location selected by the participant. A precision effect was evident in the left angular gyrus, where BOLD activity covaried across trials with location accuracy. Multi-voxel pattern analysis also revealed a significant item-level reinstatement effect for high-precision trials. There was no evidence of a retrieval success effect in the angular gyrus. BOLD activity in the hippocampus was insensitive to both success and precision. These findings are partially consistent with prior evidence that success and precision are dissociable features of memory retrieval.

Previous research has demonstrated that humans combine multiple sources of spatial information such as self-motion and landmark cues while navigating through an environment. However, it is unclear whether this involves comparing multiple representations obtained from different sources during navigation (parallel hypothesis) or building a representation first based on self-motion cues and then combining with landmarks later (serial hypothesis). We tested these two hypotheses (parallel vs serial) in an active navigation task using wireless mobile scalp EEG recordings. Participants walked through an immersive virtual hallway with or without conflicts between self-motion and landmarks (i.e., intersections) and pointed toward the starting position of the hallway. We employed the oscillatory signals recorded during mobile wireless scalp EEG as a means of identifying when participant representations based on self-motion versus landmark cues might have first emerged. We found that path segments, including intersections present early during navigation, were more strongly associated with later pointing error, regardless of when they appeared during encoding. We also found that there was sufficient information contained within the frontal-midline theta and posterior alpha oscillatory signals in the earliest segments of navigation involving intersections to decode condition (i.e., conflicting vs not conflicting). Together, these findings suggest that intersections play a pivotal role in the early development of spatial representations, suggesting that memory representations for the geometry of walked paths likely develop early during navigation, in support of the parallel hypothesis., Competing Interests: Declaration of competing interest None., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

Previous work has shown how different interfaces (i.e., route navigation, maps, or a combination of the two) influence spatial knowledge and recollection. To test for the existence of intermediate representations along an egocentric-to-allocentric continuum, we developed a novel task, tabletop navigation, to provide a mixture of cues that inform the emergence of egocentric and allocentric representations or strategies. In this novel tabletop task, participants navigated a remote-controlled avatar through a tabletop scale model of the virtual city. Participants learned virtual cities from either navigating routes, studying maps, or our new tabletop navigation task. We interleaved these learning tasks with either an in situ pointing task (the scene- and orientation-dependent pointing [SOP] task) or imagined judgements of relative direction (JRD) pointing. In Experiment 1, performance on each memory task was similar across learning tasks and performance on the route and map learning tasks correlated with more precise spatial recall on both the JRD and SOP tasks. Tabletop learning performance correlated with SOP performance only, suggesting a reliance on egocentric strategies, although increased utilization of the affordances of the tabletop task were related to JRD performance. In Experiment 2, using a modified criterion map learning task, participants who learned using maps provided more precise responses on the JRD compared to route or tabletop learning. Together, these findings provide mixed evidence for both optimization and egocentric predominance after learning from the novel tabletop navigation task., (© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Spatial navigation and memory are often seen as heavily intertwined at the cognitive and neural levels of analysis. We review models that hypothesize a central role for the medial temporal lobes, including the hippocampus, in both navigation and aspects of memory, particularly allocentric navigation and episodic memory. While these models have explanatory power in instances in which they overlap, they are limited in explaining functional and neuroanatomical differences. Focusing on human cognition, we explore the idea of navigation as a dynamically acquired skill and memory as an internally driven process, which may better account for the differences between the two. We also review network models of navigation and memory, which place a greater emphasis on connections rather than the functions of focal brain regions. These models, in turn, may have greater explanatory power for the differences between navigation and memory and the differing effects of brain lesions and age., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

When we remember a city that we have visited, we retrieve places related to finding our goal but also non-target locations within this environment. Yet, understanding how the human brain implements the neural computations underlying holistic retrieval remains unsolved, particularly for shared aspects of environments. Here, human participants learned and retrieved details from three partially overlapping environments while undergoing high-resolution functional magnetic resonance imaging (fMRI). Our findings show reinstatement of stores even when they are not related to a specific trial probe, providing evidence for holistic environmental retrieval. For stores shared between cities, we find evidence for pattern separation (representational orthogonalization) in hippocampal subfield CA2/3/DG and repulsion in CA1 (differentiation beyond orthogonalization). Additionally, our findings demonstrate that medial prefrontal cortex (mPFC) stores representations of the common spatial structure, termed schema, across environments. Together, our findings suggest how unique and common elements of multiple spatial environments are accessed computationally and neurally., (© 2021. The Author(s).)

Functional magnetic resonance imaging (fMRI) is the dominant tool in cognitive neuroscience although its relation to underlying neural activity, particularly in the human brain, remains largely unknown. A major research goal, therefore, has been to uncover a 'Rosetta Stone' providing direct translation between the blood oxygen level-dependent (BOLD) signal, the local field potential and single-neuron activity. Here, I evaluate the proposal that BOLD signal changes equate to changes in gamma-band activity, which in turn may partially relate to the spiking activity of neurons. While there is some support for this idea in sensory cortices, findings in deeper brain structures like the hippocampus instead suggest both regional and frequency-wise differences. Relatedly, I consider four important factors in linking fMRI to neural activity: interpretation of correlations between these signals, regional variability in local vasculature, distributed neural coding schemes and varying fMRI signal quality. Novel analytic fMRI techniques, such as multivariate pattern analysis (MVPA), employ the distributed patterns of voxels across a brain region to make inferences about information content rather than whether a small number of voxels go up or down relative to baseline in response to a stimulus. Although unlikely to provide a Rosetta Stone, MVPA, therefore, may represent one possible means forward for better linking BOLD signal changes to the information coded by underlying neural activity. This article is part of the theme issue 'Key relationships between non-invasive functional neuroimaging and the underlying neuronal activity'.

Experiments on rodents have demonstrated that transecting the white matter fibre pathway linking the hippocampus with an array of cortical and subcortical structures - the fornix - impairs flexible navigational learning in the Morris Water Maze (MWM), as well as similar spatial learning tasks. While diffusion magnetic resonance imaging (dMRI) studies in humans have linked inter-individual differences in fornix microstructure to episodic memory abilities, its role in human spatial learning is currently unknown. We used high-angular resolution diffusion MRI combined with constrained spherical deconvolution-based tractography, to ask whether inter-individual differences in fornix microstructure in healthy young adults would be associated with spatial learning in a virtual reality navigation task. To efficiently capture individual learning across trials, we adopted a novel curve fitting approach to estimate a single index of learning rate. We found a statistically significant correlation between learning rate and the microstructure (mean diffusivity) of the fornix, but not that of a comparison tract linking occipital and anterior temporal cortices (the inferior longitudinal fasciculus, ILF). Further, this correlation remained significant when controlling for both hippocampal volume and participant gender. These findings extend previous animal studies by demonstrating the functional relevance of the fornix for human spatial learning in a virtual reality environment, and highlight the importance of a distributed neuroanatomical network, underpinned by key white matter pathways, such as the fornix, in complex spatial behaviour., Competing Interests: Declaration of Competing Interest None., (Copyright © 2019 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as sleep to neocortical areas for long-term storage. Here, we propose an alternative to this standard systems consolidation theory (SSCT) - a contextual binding account - in which the hippocampus binds item-related and context-related information. We compare these accounts in light of behavioural, lesion, neuroimaging and sleep studies of episodic memory and contend that forgetting is largely due to contextual interference, episodic memory remains dependent on the hippocampus across time, contextual drift produces post-encoding activity and sleep benefits memory by reducing contextual interference.

The hippocampus plays a critical role in spatial and episodic memory. Mechanistic models predict that hippocampal subfields have computational specializations that differentially support memory. However, there is little empirical evidence suggesting differences between the subfields, particularly in humans. To clarify how hippocampal subfields support human spatial and episodic memory, we developed a virtual reality paradigm where participants passively navigated through houses (spatial contexts) across a series of videos (episodic contexts). We then used multivariate analyses of high-resolution fMRI data to identify neural representations of contextual information during recollection. Multi-voxel pattern similarity analyses revealed that CA1 represented objects that shared an episodic context as more similar than those from different episodic contexts. CA23DG showed the opposite pattern, differentiating between objects encountered in the same episodic context. The complementary characteristics of these subfields explain how we can parse our experiences into cohesive episodes while retaining the specific details that support vivid recollection.

Humans, like many other species, employ three fundamental forms of strategies to navigate: allocentric, egocentric, and beacon. Here, we review each of these different forms of navigation with a particular focus on how our high-resolution visual system contributes to their unique properties. We also consider how we might employ allocentric and egocentric representations, in particular, across different spatial dimensions, such as 1-D vs. 2-D. Our high acuity visual system also leads to important considerations regarding the scale of space we are navigating (e.g., smaller, room-sized "vista" spaces or larger city-sized "environmental" spaces). We conclude that a hallmark of human spatial navigation is our ability to employ these representations systems in a parallel and flexible manner, which differ both as a function of dimension and spatial scale., Competing Interests: The authors state that they have no conflicts of interest.

The ability to retain information in working memory (WM) requires not only the active maintenance of information about specific items, but also the temporal order in which the items appeared. Although many studies have investigated the neural mechanisms of item maintenance, little is known about the neural mechanisms of temporal order maintenance in WM. Here, we used electroencephalography (EEG) to compare neural oscillations during WM tasks that required maintenance of item or temporal order information. Behavioral results revealed that accuracy and reaction times were comparable between the two conditions, suggesting that task difficulty was matched between the item and temporal order WM tasks. EEG analyses indicated that theta (5-7 Hz) oscillations over prefrontal sites were increased during temporal order maintenance, whereas alpha oscillations (9-12 Hz) over posterior parietal and lateral occipital sites were increased during item maintenance. The frontal theta enhancement was primarily evident in high performers on the order WM task, whereas the posterior alpha enhancement was primarily evident in high performers on the item WM task. These results support the idea that frontal theta and posterior alpha oscillations are differentially related to maintenance of item and temporal order information.