Arne David Ekstrom

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Scholarly Contributions

Books

• Ekstrom, A. D., Spiers, H., Bohbot, V., & Rosenbaum, S. (2018). Human Spatial Navigation. Princeton University Press.

Chapters

• Ekstrom, A. D., & Ranganath, C. (2020). Maps, Memories, and the Hippocampus. In The Cognitive Neurosciences.

Journals/Publications

• Harootonian, S. K., Ekstrom, A. D., & Wilson, R. C. (2022). Combination and competition between path integration and landmark navigation in the estimation of heading direction. PLoS computational biology, 18(2), e1009222.
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  Successful navigation requires the ability to compute one's location and heading from incoming multisensory information. Previous work has shown that this multisensory input comes in two forms: body-based idiothetic cues, from one's own rotations and translations, and visual allothetic cues, from the environment (usually visual landmarks). However, exactly how these two streams of information are integrated is unclear, with some models suggesting the body-based idiothetic and visual allothetic cues are combined, while others suggest they compete. In this paper we investigated the integration of body-based idiothetic and visual allothetic cues in the computation of heading using virtual reality. In our experiment, participants performed a series of body turns of up to 360 degrees in the dark with only a brief flash (300ms) of visual feedback en route. Because the environment was virtual, we had full control over the visual feedback and were able to vary the offset between this feedback and the true heading angle. By measuring the effect of the feedback offset on the angle participants turned, we were able to determine the extent to which they incorporated visual feedback as a function of the offset error. By further modeling this behavior we were able to quantify the computations people used. While there were considerable individual differences in performance on our task, with some participants mostly ignoring the visual feedback and others relying on it almost entirely, our modeling results suggest that almost all participants used the same strategy in which idiothetic and allothetic cues are combined when the mismatch between them is small, but compete when the mismatch is large. These findings suggest that participants update their estimate of heading using a hybrid strategy that mixes the combination and competition of cues.
• Ekstrom, A. D. (2021). Regional variation in neurovascular coupling and why we still lack a Rosetta Stone. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 376(1815), 20190634.
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  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'.
• Ekstrom, A. D., & Weisberg, S. (2021). Hippocampal volume and navigational ability: The map(ping) is not to scale.. Neuroscience and Biobehavioral Reviews.
• Huffman, D. J., Huffman, D. J., Ekstrom, A. D., & Ekstrom, A. D. (2021). An Important Step toward Understanding the Role of Body-based Cues on Human Spatial Memory for Large-Scale Environments. Journal of cognitive neuroscience, 33(2), 167-179.
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  Moving our body through space is fundamental to human navigation; however, technical and physical limitations have hindered our ability to study the role of these body-based cues experimentally. We recently designed an experiment using novel immersive virtual-reality technology, which allowed us to tightly control the availability of body-based cues to determine how these cues influence human spatial memory [Huffman, D. J., & Ekstrom, A. D. A modality-independent network underlies the retrieval of large-scale spatial environments in the human brain. , , 611-622, 2019]. Our analysis of behavior and fMRI data revealed a similar pattern of results across a range of body-based cues conditions, thus suggesting that participants likely relied primarily on vision to form and retrieve abstract, holistic representations of the large-scale environments in our experiment. We ended our paper by discussing a number of caveats and future directions for research on the role of body-based cues in human spatial memory. Here, we reiterate and expand on this discussion, and we use a commentary in this issue by A. Steel, C. E. Robertson, and J. S. Taube (Current promises and limitations of combined virtual reality and functional magnetic resonance imaging research in humans: A commentary on Huffman and Ekstrom (2019). , 2020) as a helpful discussion point regarding some of the questions that we think will be the most interesting in the coming years. We highlight the exciting possibility of taking a more naturalistic approach to study the behavior, cognition, and neuroscience of navigation. Moreover, we share the hope that researchers who study navigation in humans and nonhuman animals will synergize to provide more rapid advancements in our understanding of cognition and the brain.
• Izadi, A., Pevzner, A., Lee, D. J., Ekstrom, A. D., Shahlaie, K., & Gurkoff, G. G. (2019). Medial septal stimulation increases seizure threshold and improves cognition in epileptic rats. Brain stimulation, 12(3), 735-742.
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  Temporal lobe epilepsy is most prevalent among focal epilepsies, and nearly one-third of patients are refractory to pharmacological intervention. Persistent cognitive and neurobehavioral comorbidities also occur due to the recurrent nature of seizures and medication-related side effects.
• Izadi, A., Schedlbauer, A., Ondek, K., Disse, G., Ekstrom, A. D., Cowen, S. L., Shahlaie, K., & Gurkoff, G. G. (2021). Early Intervention via Stimulation of the Medial Septal Nucleus Improves Cognition and Alters Markers of Epileptogenesis in Pilocarpine-Induced Epilepsy. Frontiers in neurology, 12, 708957.
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  Over one-third of patients with temporal lobe epilepsy are refractory to medication. In addition, anti-epileptic drugs often exacerbate cognitive comorbidities. Neuromodulation is an FDA treatment for refractory epilepsy, but patients often wait >20 years for a surgical referral for resection or neuromodulation. Using a rodent model, we test the hypothesis that 2 weeks of theta stimulation of the medial septum acutely following exposure to pilocarpine will alter the course of epileptogenesis resulting in persistent behavioral improvements. Electrodes were implanted in the medial septum, dorsal and ventral hippocampus, and the pre-frontal cortex of pilocarpine-treated rats. Rats received 30 min/day of 7.7 Hz or theta burst frequency on days 4-16 post-pilocarpine, prior to the development of spontaneous seizures. Seizure threshold, spikes, and oscillatory activity, as well as spatial and object-based learning, were assessed in the weeks following stimulation. Non-stimulated pilocarpine animals exhibited significantly decreased seizure threshold, increased spikes, and cognitive impairments as compared to vehicle controls. Furthermore, decreased ventral hippocampal power (6-10 Hz) correlated with both the development of spikes and impaired cognition. Measures of spikes, seizure threshold, and cognitive performance in both acute 7.7 Hz and theta burst stimulated animals were statistically similar to vehicle controls when tested during the chronic phase of epilepsy, weeks after stimulation was terminated. These data indicate that modulation of the septohippocampal circuit early after pilocarpine treatment alters the progression of epileptic activity, resulting in elevated seizure thresholds, fewer spikes, and improved cognitive outcome. Results from this study support that septal theta stimulation has the potential to serve in combination or as an alternative to high frequency thalamic stimulation in refractory cases and that further research into early intervention is critical.
• Liang, M., Isham, E. A., Zheng, J., & Ekstrom, A. D. (2021). Common and distinct roles of frontal midline theta and occipital alpha oscillations in coding temporal intervals and spatial distances.. Journal of Cognitive Neuroscience.
• McAvan, A., Du, Y., Alexis, O., Stephanie, D., Grilli, M. D., & Ekstrom, A. D. (2021). Older adults show reduced spatial precision but preserved strategy use during spatial navigation involving body-based cues.. Frontiers in Neurobiology of Aging.
• Preciado, C., Starrett, M. J., & Ekstrom, A. D. (2021). Short, focused training in virtual reality does not reduce symptoms of cybersickness.. Presence.
• Suthana, N., Ekstrom, A. D., Yassa, M., & Craig, S. (2021). Pattern separation in the human hippocampus: Response to Quiroga. Trends in Cognitive Sciences.
• Zheng, J., Liang, M., Sinha, S., Ge, L., Yu, W., Ekstrom, A., & Hsieh, F. (2021). time-frequency analysis of scalp EEG with Hilbert-Huang transform and deep learning. IEEE journal of biomedical and health informatics, PP.
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  Electroencephalography (EEG) is a brain imaging approach that has been widely used in neuroscience and clinical settings. The conventional EEG analyses usually require pre-defined frequency bands when characterizing neural oscillations and extracting features for classifying EEG signals. However, neural responses are naturally heterogeneous by showing variations in frequency bands of brainwaves and peak frequencies of oscillatory modes across individuals. Fail to account for such variations might result in information loss and classifiers with low accuracy but high variation across individuals. To address these issues, we present a systematic time-frequency analysis approach for analyzing scalp EEG signals. In particular, we propose a data-driven method to compute the subject-specific frequency bands for brain oscillations via Hilbert-Huang Transform, lifting the restriction of using fixed frequency bands for all subjects. Then, we propose two novel metrics to quantify the power and frequency aspects of brainwaves represented by sub-signals decomposed from the EEG signals. The effectiveness of the proposed metrics are tested on two scalp EEG datasets and compared with four commonly used features sets extracted from wavelet and Hilbert-Huang Transform. The validation results show that the proposed metrics are more discriminatory than other features leading to accuracies in the range of 94.93% to 99.84%. Besides classification, the proposed metrics show great potential in quantification of neural oscillations and serving as biomarkers in the neuroscience research.
• Zheng, L., Gao, Z., McAvan, A. S., Isham, E. A., & Ekstrom, A. D. (2021). Partially overlapping spatial environments trigger reinstatement in hippocampus and schema representations in prefrontal cortex. Nature communications, 12(1), 6231.
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  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.
• Ekstrom, A. D. (2020). Cognitive Neuroscience: Why Do We Get Lost When We Are Stressed?. Current biology : CB, 30(10), R439-R441.
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  A recent study in humans shows that stress increases our reliance on familiar routes during navigation. This research explains how increases in cortisol, a biomarker of stress, disrupts navigation-related brain circuits, resulting in less efficient navigation.
• Ekstrom, A. D., & Yonelinas, A. P. (2020). Precision, binding, and the hippocampus: Precisely what are we talking about?. Neuropsychologia, 138, 107341.
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  Endel Tulving's proposal that episodic memory is distinct from other memory systems like semantic memory remains an extremely influential idea in cognitive neuroscience research. As originally suggested by Tulving, episodic memory involves three key components that differentiate it from all other memory systems: spatiotemporal binding, mental time travel, and autonoetic consciousness. Here, we focus on the idea of spatiotemporal binding in episodic memory and, in particular, how consideration of the precision of spatiotemporal context helps expand our understanding of episodic memory. Precision also helps shed light on another key issue in cognitive neuroscience, the role of the hippocampus outside of episodic memory in perception, attention, and working memory. By considering precision alongside item-context bindings, we attempt to shed new light on both the nature of how we represent context and what roles the hippocampus plays in episodic memory and beyond.
• Ekstrom, A. D., Harootonian, S. K., & Huffman, D. J. (2020). Grid coding, spatial representation, and navigation: Should we assume an isomorphism?. Hippocampus, 30(4), 422-432.
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  Grid cells provide a compelling example of a link between cellular activity and an abstract and difficult to define concept like space. Accordingly, a representational perspective on grid coding argues that neural grid coding underlies a fundamentally spatial metric. Recently, some theoretical proposals have suggested extending such a framework to nonspatial cognition as well, such as category learning. Here, we provide a critique of the frequently employed assumption of an isomorphism between patterns of neural activity (e.g., grid cells), mental representation, and behavior (e.g., navigation). Specifically, we question the strict isomorphism between these three levels and suggest that human spatial navigation is perhaps best characterized by a wide variety of both metric and nonmetric strategies. We offer an alternative perspective on how grid coding might relate to human spatial navigation, arguing that grid coding is part of a much larger conglomeration of neural activity patterns that dynamically tune to accomplish specific behavioral outputs.
• Harootonian, S. K., Wilson, R. C., Hejtmánek, L., Ziskin, E. M., & Ekstrom, A. D. (2020). Path integration in large-scale space and with novel geometries: Comparing vector addition and encoding-error models. PLoS computational biology, 16(5), e1007489.
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  Path integration is thought to rely on vestibular and proprioceptive cues yet most studies in humans involve primarily visual input, providing limited insight into their respective contributions. We developed a paradigm involving walking in an omnidirectional treadmill in which participants were guided on two sides of a triangle and then found their back way to origin. In Experiment 1, we tested a range of different triangle types while keeping the distance of the unguided side constant to determine the influence of spatial geometry. Participants overshot the angle they needed to turn and undershot the distance they needed to walk, with no consistent effect of triangle type. In Experiment 2, we manipulated distance while keeping angle constant to determine how path integration operated over both shorter and longer distances. Participants underestimated the distance they needed to walk to the origin, with error increasing as a function of the walked distance. To attempt to account for our findings, we developed configural-based computational models involving vector addition, the second of which included terms for the influence of past trials on the current one. We compared against a previously developed configural model of human path integration, the Encoding-Error model. We found that the vector addition models captured the tendency of participants to under-encode guided sides of the triangles and an influence of past trials on current trials. Together, our findings expand our understanding of body-based contributions to human path integration, further suggesting the value of vector addition models in understanding these important components of human navigation.
• Hejtmanek, L., Starrett, M., Ferrer, E., & Ekstrom, A. D. (2020). How Much of What We Learn in Virtual Reality Transfers to Real-World Navigation?. Multisensory research, 33(4-5), 479-503.
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  Past studies suggest that learning a spatial environment by navigating on a desktop computer can lead to significant acquisition of spatial knowledge, although typically less than navigating in the real world. Exactly how this might differ when learning in immersive virtual interfaces that offer a rich set of multisensory cues remains to be fully explored. In this study, participants learned a campus building environment by navigating (1) the real-world version, (2) an immersive version involving an omnidirectional treadmill and head-mounted display, or (3) a version navigated on a desktop computer with a mouse and a keyboard. Participants first navigated the building in one of the three different interfaces and, afterward, navigated the real-world building to assess information transfer. To determine how well they learned the spatial layout, we measured path length, visitation errors, and pointing errors. Both virtual conditions resulted in significant learning and transfer to the real world, suggesting their efficacy in mimicking some aspects of real-world navigation. Overall, real-world navigation outperformed both immersive and desktop navigation, effects particularly pronounced early in learning. This was also suggested in a second experiment involving transfer from the real world to immersive virtual reality (VR). Analysis of effect sizes of going from virtual conditions to the real world suggested a slight advantage for immersive VR compared to desktop in terms of transfer, although at the cost of increased likelihood of dropout. Our findings suggest that virtual navigation results in significant learning, regardless of the interface, with immersive VR providing some advantage when transferring to the real world.
• Hodgetts, C. J., Stefani, M., Williams, A. N., Kolarik, B. S., Yonelinas, A. P., Ekstrom, A. D., Lawrence, A. D., Zhang, J., & Graham, K. S. (2020). The role of the fornix in human navigational learning. Cortex; a journal devoted to the study of the nervous system and behavior, 124, 97-110.
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  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.
• Ondek, K., Pevzner, A., Tercovich, K., Schedlbauer, A. M., Izadi, A., Ekstrom, A. D., Cowen, S. L., Shahlaie, K., & Gurkoff, G. G. (2020). Recovery of Theta Frequency Oscillations in Rats Following Lateral Fluid Percussion Corresponds With a Mild Cognitive Phenotype. Frontiers in neurology, 11, 600171.
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  Whether from a fall, sports concussion, or even combat injury, there is a critical need to identify when an individual is able to return to play or work following traumatic brain injury (TBI). Electroencephalogram (EEG) and local field potentials (LFP) represent potential tools to monitor circuit-level abnormalities related to learning and memory: specifically, theta oscillations can be readily observed and play a critical role in cognition. Following moderate traumatic brain injury in the rat, lasting changes in theta oscillations coincide with deficits in spatial learning. We hypothesized, therefore, that theta oscillations can be used as an objective biomarker of recovery, with a return of oscillatory activity corresponding with improved spatial learning. In the current study, LFP were recorded from dorsal hippocampus and anterior cingulate in awake, behaving adult Sprague Dawley rats in both a novel environment on post-injury days 3 and 7, and Barnes maze spatial navigation on post-injury days 8-11. Theta oscillations, as measured by power, theta-delta ratio, peak theta frequency, and phase coherence, were significantly altered on day 3, but had largely recovered by day 7 post-injury. Injured rats had a mild behavioral phenotype and were not different from shams on the Barnes maze, as measured by escape latency. Injured rats did use suboptimal search strategies. Combined with our previous findings that demonstrated a correlation between persistent alterations in theta oscillations and spatial learning deficits, these new data suggest that neural oscillations, and particularly theta oscillations, have potential as a biomarker to monitor recovery of brain function following TBI. Specifically, we now demonstrate that oscillations are depressed following injury, but as oscillations recover, so does behavior.
• Starrett, M. J., McAvan, A. S., Huffman, D. J., Stokes, J. D., Kyle, C. T., Smuda, D. N., Kolarik, B. S., Laczko, J., & Ekstrom, A. D. (2020). Landmarks: A solution for spatial navigation and memory experiments in virtual reality. Behavior research methods.
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  Research into the behavioral and neural correlates of spatial cognition and navigation has benefited greatly from recent advances in virtual reality (VR) technology. Devices such as head-mounted displays (HMDs) and omnidirectional treadmills provide research participants with access to a more complete range of body-based cues, which facilitate the naturalistic study of learning and memory in three-dimensional (3D) spaces. One limitation to using these technologies for research applications is that they almost ubiquitously require integration with video game development platforms, also known as game engines. While powerful, game engines do not provide an intrinsic framework for experimental design and require at least a working proficiency with the software and any associated programming languages or integrated development environments (IDEs). Here, we present a new asset package, called Landmarks, for designing and building 3D navigation experiments in the Unity game engine. Landmarks combines the ease of building drag-and-drop experiments using no code, with the flexibility of allowing users to modify existing aspects, create new content, and even contribute their work to the open-source repository via GitHub, if they so choose. Landmarks is actively maintained and is supplemented by a wiki with resources for users including links, tutorials, videos, and more. We compare several alternatives to Landmarks for building navigation experiments and 3D experiments more generally, provide an overview of the package and its structure in the context of the Unity game engine, and discuss benefits relating to the ongoing and future development of Landmarks.
• Woolnough, O., Rollo, P. S., Forseth, K. J., Kadipasaoglu, C. M., Ekstrom, A. D., & Tandon, N. (2020). Category Selectivity for Face and Scene Recognition in Human Medial Parietal Cortex. Current biology : CB, 30(14), 2707-2715.e3.
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  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.
• Huffman, D. J., & Ekstrom, A. D. (2019). A Modality-Independent Network Underlies the Retrieval of Large-Scale Spatial Environments in the Human Brain. Neuron, 104(3), 611-622.e7.
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  In humans, the extent to which body-based cues, such as vestibular, somatosensory, and motoric cues, are necessary for normal expression of spatial representations remains unclear. Recent breakthroughs in immersive virtual reality technology allowed us to test how body-based cues influence spatial representations of large-scale environments in humans. Specifically, we manipulated the availability of body-based cues during navigation using an omnidirectional treadmill and a head-mounted display, investigating brain differences in levels of activation (i.e., univariate analysis), patterns of activity (i.e., multivariate pattern analysis), and putative network interactions between spatial retrieval tasks using fMRI. Our behavioral and neuroimaging results support the idea that there is a core, modality-independent network supporting spatial memory retrieval in the human brain. Thus, for well-learned spatial environments, at least in humans, primarily visual input may be sufficient for expression of complex representations of spatial environments. VIDEO ABSTRACT.
• Huffman, D. J., & Ekstrom, A. D. (2019). Which way is the bookstore? A closer look at the judgments of relative directions task. Spatial cognition and computation, 19(2), 93-129.
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  We present a detailed analysis of a widely used assay in human spatial cognition, the judgments of relative direction (JRD) task. We conducted three experiments involving virtual navigation interspersed with the JRD task, and included confidence judgments and map drawing as additional metrics. We also present a technique for assessing the similarity of the cognitive representations underlying performance on the JRD and map drawing tasks. Our results support the construct validity of the JRD task and its connection to allocentric representation. Additionally, we found that chance performance on the JRD task depends on the distribution of the angles of participants' responses, rather than being constant and 90 degrees. Accordingly, we present a method for better determining chance performance.
• Peacock, C. E., & Ekstrom, A. D. (2019). Verbal cues flexibly transform spatial representations in human memory. Memory (Hove, England), 27(4), 465-479.
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  Humans possess a unique ability to communicate spatially-relevant information, yet the intersection between language and navigation remains largely unexplored. One possibility is that verbal cues accentuate heuristics useful for coding spatial layouts, yet this idea remains largely untested. We test the idea that verbal cues flexibly accentuate the coding of heuristics to remember spatial layouts via spatial boundaries or landmarks. The alternative hypothesis instead conceives of encoding during navigation as a step-wise process involving binding lower-level features, and thus subsequently formed spatial representations should not be modified by verbal cues. Across three experiments, we found that verbal cues significantly affected pointing error patterns at axes that were aligned with the verbally cued heuristic, suggesting that verbal cues influenced the heuristics employed to remember object positions. Further analyses suggested evidence for a hybrid model, in which boundaries were encoded more obligatorily than landmarks, but both were accessed flexibly with verbal instruction. These findings could not be accounted for by a tendency to spend more time facing the instructed component during navigation, ruling out an attentional-encoding mechanism. Our findings argue that verbal cues influence the heuristics employed to code environments, suggesting a mechanism for how humans use language to communicate navigationally-relevant information.
• Schedlbauer, A. M., & Ekstrom, A. D. (2019). Flexible network community organization during the encoding and retrieval of spatiotemporal episodic memories. Network neuroscience (Cambridge, Mass.), 3(4), 1070-1093.
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  Memory encoding and retrieval involve distinct interactions between multiple brain areas, yet the flexible structure of corresponding large-scale networks during such memory processing remains unclear. Using functional magnetic resonance imaging, we employed a spatiotemporal encoding and retrieval task, detecting functional community structure across the multiple components of our task. Consistent with past work, we identified a set of stable subnetworks, mostly belonging to primary motor and sensory cortices but also identified a subset of flexible hubs, mostly belonging to higher association areas. These "mover" hubs changed connectivity patterns across spatial and temporal memory encoding and retrieval, engaging in an integrative role within the network. Global encoding network and subnetwork dissimilarity predicted retrieval performance. Together, our findings emphasize the importance of flexible network allegiance among some hubs and the importance of network reconfiguration to human episodic memory.
• Starrett, M. J., Stokes, J. D., Huffman, D. J., Ferrer, E., & Ekstrom, A. D. (2019). Learning-dependent evolution of spatial representations in large-scale virtual environments. Journal of experimental psychology. Learning, memory, and cognition, 45(3), 497-514.
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  An important question regards how we use environmental boundaries to anchor spatial representations during navigation. Behavioral and neurophysiological models appear to provide conflicting predictions, and this question has been difficult to answer because of technical challenges with testing navigation in novel, large-scale, realistic spatial environments. We conducted an experiment in which participants freely ambulated on an omnidirectional treadmill while viewing novel, town-sized environments in virtual reality on a head-mounted display. Participants performed interspersed judgments of relative direction (JRD) to assay their spatial knowledge and to determine when during learning they employed environmental boundaries to anchor their spatial representations. We designed JRD questions that assayed directions aligned and misaligned with the axes of the surrounding rectangular boundaries and employed structural equation modeling to better understand the learning-dependent dynamics for aligned versus misaligned pointing. Pointing accuracy showed no initial directional bias to boundaries, although such "alignment effects" did emerge after the fourth block of learning. Preexposure to a map in Experiment 2 led to similar overall findings. A control experiment in which participants studied a map but did not navigate the environment, however, demonstrated alignment effects after a brief, initial learning experience. Our results help to bridge the gap between neurophysiological models of location-specific firing in rodents and human behavioral models of spatial navigation by emphasizing the experience-dependent accumulation of route-specific knowledge. In particular, our results suggest that the use of spatial boundaries as an organizing schema during navigation of large-scale space occurs in an experience-dependent fashion. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
• Yonelinas, A. P., Ranganath, C., Ekstrom, A. D., & Wiltgen, B. J. (2019). A contextual binding theory of episodic memory: systems consolidation reconsidered. Nature reviews. Neuroscience, 20(6), 364-375.
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  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.
• Yonelinas, A. P., Ranganath, C., Ekstrom, A. D., & Wiltgen, B. J. (2019). Reply to 'Active and effective replay: systems consolidation reconsidered again'. Nature reviews. Neuroscience, 20(8), 507-508.
• Arnold, A. E., Ekstrom, A. D., & Iaria, G. (2018). Dynamic Neural Network Reconfiguration During the Generation and Reinstatement of Mnemonic Representations. Frontiers in human neuroscience, 12, 292.
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  Mnemonic representations allow humans to re-experience the past or simulate future scenarios by integrating episodic features from memory. Theoretical models posit that mnemonic representations require dynamic processing between neural indexes in the hippocampus and areas of the cortex providing specialized information processing. However, it remains unknown whether global and local network topology varies as information is encoded into a mnemonic representation and subsequently reinstated. Here, we investigated the dynamic nature of memory networks while a representation of a virtual city is generated and reinstated during mental simulations. We find that the brain reconfigures from a state of heightened integration when encoding demands are highest, to a state of localized processing once representations are formed. This reconfiguration is associated with changes in hippocampal centrality at the intra- and inter-module level, decreasing its role as a connector hub between modules and within a hippocampal neighborhood as encoding demands lessen. During mental simulations, we found increased levels of hippocampal centrality within its local neighborhood coupled with decreased functional interactions between other regions of the neighborhood during highly vivid simulations, suggesting that information flow vis-à-vis the hippocampus is critical for high fidelity recapitulation of mnemonic representations.
• Dimsdale-Zucker, H. R., Ritchey, M., Ekstrom, A. D., Yonelinas, A. P., & Ranganath, C. (2018). CA1 and CA3 differentially support spontaneous retrieval of episodic contexts within human hippocampal subfields. Nature communications, 9(1), 294.
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  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.
• Ekstrom, A. D., Le, C., & Isham, E. A. (2018). Rightward and leftward biases in temporal reproduction of objects represented in central and peripheral spaces.. Neurobiology of Learning and Memory. doi:https://doi.org/10.1016/j.nlm.2017.12.006
• Isham, E. A., Le, C. H., & Ekstrom, A. D. (2018). Rightward and leftward biases in temporal reproduction of objects represented in central and peripheral spaces. Neurobiology of learning and memory, 153(Pt A), 71-78.
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  The basis for how we represent temporal intervals in memory remains unclear. One proposal, the mental time line theory (MTL), posits that our representation of temporal duration depends on a horizontal mental time line, thus suggesting that the representation of time has an underlying spatial component. Recent work suggests that the MTL is a learned strategy, prompting new questions of when and why MTL is used to represent temporal duration, and whether time is always represented spatially. The current study examines the hypothesis that the MTL may be a time processing strategy specific to centrally-located stimuli. In two experiments (visual eccentricity and prismatic adaptation procedures), we investigated the magnitude of the rightward bias, an index of the MTL, in central and peripheral space. When participants performed a supra-second temporal interval reproduction task, we observed a rightward bias only in central vision (within 3° visual angle), but not in the peripheral space (approximately 6-8° visual angle). Instead, in the periphery, we observed a leftward bias. The results suggest that the MTL may be a learned strategy specific to central space and that strategies for temporal interval estimation that do not depend on MTL may exist for stimuli perceived peripherally.
• Liang, M., Starrett, M. J., & Ekstrom, A. D. (2018). Dissociation of frontal-midline delta-theta and posterior alpha oscillations: A mobile EEG study. Psychophysiology, 55(9), e13090.
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  Numerous reports have demonstrated low-frequency oscillations during navigation using invasive recordings in the hippocampus of both rats and human patients. Given evidence, in some cases, of low-frequency synchronization between midline cortex and hippocampus, it is also possible that low-frequency movement-related oscillations manifest in healthy human neocortex. However, this possibility remains largely unexplored, in part due to the difficulties of coupling free ambulation and effective scalp EEG recordings. In the current study, participants freely ambulated on an omnidirectional treadmill and explored an immersive virtual reality city rendered on a head-mounted display while undergoing simultaneous wireless scalp EEG recordings. We found that frontal-midline (FM) delta-theta (2-7.21 Hz) oscillations increased during movement compared to standing still periods, consistent with a role in navigation. In contrast, posterior alpha (8.32-12.76 Hz) oscillations were suppressed in the presence of visual input, independent of movement. Our findings suggest that FM delta-theta and posterior alpha oscillations arise at independent frequencies, under complementary behavioral conditions, and, at least for FM delta-theta oscillations, at independent recordings sites. Together, our findings support a double dissociation between movement-related FM delta-theta and resting-related posterior alpha oscillations. Our study thus provides novel evidence that FM delta-theta oscillations arise, in part, from real-world ambulation, and are functionally independent from posterior alpha oscillations.
• Starrett, M. J., & Ekstrom, A. D. (2018). Perspective: Assessing the Flexible Acquisition, Integration, and Deployment of Human Spatial Representations and Information. Frontiers in human neuroscience, 12, 281.
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  Studying human spatial navigation in the lab can be challenging, particularly when including non-invasive neural measures like functional magnetic resonance imaging (fMRI) and scalp encephalography (EEG). While there is broad consensus that human spatial navigation involves both egocentric (self-referenced) and allocentric (world-referenced) coding schemes, exactly how these can be measured in ecologically meaningful situations remains controversial. Here, we explore these two forms of representation and how we might better measure them by reviewing commonly used spatial memory tasks and proposing a new task: the relative vector discrimination (RVD) task. Additionally, we explore how different encoding modalities (desktop virtual reality, immersive virtual reality, maps, and real-world navigation) might alter how egocentric and allocentric representations manifest. Specifically, we discuss desktop virtual reality vs. more immersive forms of navigation that better approximate real-world situations, and the extent to which less immersive encoding modalities alter neural and cognitive codes engaged during navigation more generally. We conclude that while encoding modality likely alters navigation-related codes to some degree, including egocentric and allocentric representations, it does not fundamentally change the underlying representations. Considering these arguments together, we suggest that tools to study human navigation in the lab, such as desktop virtual reality, provide overall a reasonable approximation of navigation, with some caveats.
• Isham, E. A., & Ekstrom, A. D. (2017). Human spatial navigation: Representations across dimensions and scales.. Current Opinion in Behavioral Sciences, 17, 84-89. doi:DOI: http://dx.doi.org/10.1016/j.cobeha.2017.06.005
• Banks, W. P., Ekstrom, A. D., & Isham, E. A. (2010). Effects of youth authorship on the appraisal of paintings. Psychology of Aesthetics, Creativity, and the Arts, 4, 235-246.

Presentations

• Ekstrom, A. D. (2021). Navigating hallways involves reconstructive memory errors in violation of Euclidean axioms. Memory Disorders Research Society.
• Ekstrom, A. D. (2021, January). Human spatial navigation and the study of human memory in the context of space. University of Arizona Neuroscience Program Data Blitz. University of Arizona (virtual).
• Ekstrom, A. D. (2020, January). Google instructional video for google engineers. Instructional film. University of Arizona: Google.
• Ekstrom, A. D. (2020, June). Human spatial navigation and episodic memory: Inspiration and divergence from rodent neural models. Presentation to University of Magdeburg Psychology Department. Magdeburg, Germany (virtual).
• Ekstrom, A. D. (2020, May). How do we represent space when we “navigate?”. UC Davis Memory Meeting. Davis, CA (virtual).
• Ekstrom, A. D. (2020, October). Immersive virtual reality and its potential applications in clinical science. UA Medical School / Phoenix. Phoenix.
• Harootonian, S., Ekstrom, A. D., & Wilson, R. C. (2020, September). A sampling model of multimodal spatial orientation. iNav (on-line).
• Ekstrom, A. D. (2018, October). Networks models of navigation and memory: What do we gain and why?. Ebbinghaus Empire Presentation. University of Toronto.
• Ekstrom, A. D. (2019, April). Navigation deficits in aging: What we can learn from (immersive) virtual reality. McKnight Brain Conference. Gainesville, FL: University of Florida.
• Ekstrom, A. D. (2019, January). Human spatial navigation and the study of human memory in the context of space. University of Arizona Neuroscience Data Blitz.
• Ekstrom, A. D. (2019, January). The neural basis of human spatial navigation: Inspiration and divergence from rodent models. University of Arizona Neuroscience Speaker Series.
• Ekstrom, A. D. (2019, October). Space and time involve partially overlapping and unique neural signatures. Time Research Forum. Queretero, Mexico.
• Ekstrom, A. D. (2019, October). Testing the influence of enriched body-based cues on how we encode and retrieve space. Memory Disorders Research Society. New York.
• Ekstrom, A. D. (2019, September). Human spatial navigation and episodic memory: Inspiration and divergence from rodent neural models. University of Arizona Psychology Colloquium Series.
• Ekstrom, A. D. (2019, September). Navigation and virtual reality. Presentation to Phoenix arts, science, and cultural salon. Phoenix, AZ.
• Liang, M., & Ekstrom, A. D. (2019, September). Wireless scalp EEG and immersive virtual interfaces provide novel insight into the neural basis of human spatial navigation.. Society for Psychophysiology Research. Washington, DC.
• Ekstrom, A. D. (2018, February). How Virtual and Altered Reality Can Help Us Understand the Neural Basis of Human Spatial Navigation. Evelyn McKnight Brain Conference. University of Arizona Medical Center: McKnight Brain Organization.
• Ekstrom, A. D. (2018, January). Navigating a virtually-immersed world: How VR/AR can help us to better understand the neural basis of human spatial navigation. UC Davis AR / VR conference. University of California, Davis Center for Mind and Brain.
• Ekstrom, A. D. (2018, June). How Virtual and Altered Reality Can Help Us Understand the Neural Basis of Human Spatial Navigation. iNav. Montreal, Quebec, Canada.
• Ekstrom, A. D. (2018, June). Navigating a virtually-immersed world: How VR/AR can help us to better understand the neural basis of human spatial navigation. University of Rochester Center for Visual Sciences Symposium. Rochester, NY.
• Ekstrom, A. D. (2018, October). Networks models of navigation and memory: What do we gain and why?. Cognitive Science Colloquium. University of Arizona.
• Ekstrom, A. D. (2018, October). What Virtual and Altered Reality Can Teach Us About How We Navigate and Remember. Industrial Engineering Fall Speaker Series. University of Arizona.
• Ekstrom, A. D. (2018, September). Brain networks for representing space, temporal order, and spatiotemporal conjunctions. Memory Disorders Research Symposium. Toronto, Canada.
• Ekstrom, A. D. (2018, September). How Virtual and Altered Reality Can Help Us Understand the Neural Basis of Human Spatial Navigation. Interpreting the BOLD signal. Oxford, England (remote).
• Ekstrom, A. D. (2018, September). Human spatial navigation and episodic memory: Inspiration and divergence from rodent neural models. Psychology Colloquium Series. University of Arizona.
• Hejtmanek, L., Starrett, M. J., & Ekstrom, A. D. (2018, June). Enriched body-based cues and transfer to real-world environments. iNav. Montreal, Quebec, Canada.
• Huffman, D., & Ekstrom, A. D. (2018, June). The effect of body-based cues on human neural representations for space following active navigation. iNav. Montreal, Quebec, Canada.
• Stern, J., Ekstrom, A. D., Banks, W., Geng, J., & Isham, E. A. (2011, July). Isham,Fame and Fortune: External Information Guides Perception.. Cognitive Science Association for Interdisciplinary Learning,. Hood River, OR.
• Aarons, B., Patel, D., Chiang, A., Copara, M., Isham, E. A., & Ekstrom, A. D. (2010, July). Ekstrom, A.D., Isham, E.A., Copara, M., Chiang, A., Patel, D., & Aarons, B. (2010, July). Independent and Conjunctive Processing of Spatial and Temporal Information in Episodic Memory. R.. Cognitive Science Association for Interdisciplinary Learning,. Hood River, OR.

Poster Presentations

• Starrett, M., Huffman, D., & Ekstrom, A. D. (2021, January). Spatial learning through interaction: A hybrid “route” to a cognitive map. Society for Neuroscience (virtual).
• Ekstrom, A. D., & Huffman, D. (2019, November). A modality-independent network underlies the retrieval of large-scale spatial environments in the human brain. Society for Neuroscience. Chicago, IL.
• Kyle, C., Stokes, J., Meltzer, J., Permenter, M., Vogt, J., Ekstrom, A. D., & Barnes, C. A. (2019, November). Convolutional neural networks for fast and accurate 3D reconstruction of histological sections. Society for Neuroscience. Chicago, IL.
• Liang, M., Ekstrom, A. D., Harootonian, S., Drake, K. W., Isham, E. A., Isham, E. A., Harootonian, S., Drake, K. W., Liang, M., & Ekstrom, A. D. (2019, November). Low-frequency neural oscillations code distance and temporal duration as measured with scalp EEG and hippocampal intracranial recordings.. Society for Neuroscience. Chicago, IL.
• Oyao, A., Du, Y. (., & Ekstrom, A. D. (2019, November). Asymmetrical influence of visual gain changes on spatial representations during navigation.. Psychonomics Society. Montreal, Quebec, Canada.
• Oyao, A., Forloines, M., Robertson, A., Grilli, M. D., & Ekstrom, A. D. (2019, November). Older adults show impairments in learning new spatial environments compared to younger adult.. Psychonomics Society. Montreal, Quebec, Canada.
• Postans, M., Williams, A., Stefani, M., Lissaman, R., Kolarik, B., Yonelinas, A., Lawrence, A., Ekstrom, A. D., Zhan, J., Graham, K., & Hodgetts, C. (2019, November). The role of the pre-commissural fornix in an extended neuroanatomical network for goal-directed navigation.. Society for Neuroscience. Chicago, IL.
• Forloines, M., Hejtmanek, L., Ochoa, D., Ober, B., & Ekstrom, A. D. (2018, November). Variations in the Flexible Use of Environment-Specific Representations in Aging. Society for Neuroscience.
• Harootonian, S., Wilson, R. C., Ziskin, E., Erlenbach, E., & Ekstrom, A. D. (2018, November). Modeling path integration in large-scale space and with novel geometries. Society for Neuroscience.
• Harootonian, S., Ziskin, E., Hejtmanek, L., Erlenbach, E., & Ekstrom, A. D. (2018, June). Path integration in large-scale space and with novel geometries. iNav. Montreal, Quebec, Canada.
• Liang, M., Starrett, M. J., & Ekstrom, A. D. (2018, June). Do cortical theta oscillations code distance, time, or both?. iNav. Montreal, Quebec, Canada.
• Liang, M., Starrett, M., & Ekstrom, A. D. (2018, November). Human frontal delta-theta dynamics code distance and time inside teleporters. Society for Neuroscience.
• Ekstrom, A. D., Geng, J., Aarons, B., Mineyev, S., Patel, D., DiQuattro, N., Copara, M., & Isham, E. A. (2010, November). Independent and conjunctive processing of spatial and temporal information in episodic memory.. SfN. San Diego, CA.

Others

• Frassinetti, F., Ekstrom, A. D., & Isham, E. A. (2019, November). Time and Space symposium.
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  Symposium organizer/chairSpeakers include:Arne EkstromFrancesca Frassinetti