Combining egoformative and alloformative cues in a novel tabletop navigation task.

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.

Attention Biases Competition for Visual Representation via Dissociable Influences from Frontal and Parietal Cortex.

What mechanisms underlie the prioritization of neural representations of visually perceived information to guide behavior? We assessed the dynamics whereby attention biases competition for representation of visual stimuli by enhancing representations of relevant information and suppressing the irrelevant. Multivariate pattern analysis (MVPA) classifiers were trained to discriminate patterns of fMRI activity associated with each of three stimuli, within several predefined ROIs. Participants performed a change-detection task wherein two of three presented items flashed at 1 Hz, one to each side of central fixation. Both flashing stimuli would unpredictably change state, but participants covertly counted the number of changes only for the cued item. In the ventral occipito-temporal ROI, MVPA evidence (a proxy for representational fidelity) was dynamically enhanced for attended stimuli and suppressed for unattended stimuli, consistent with a mechanism of biased competition between stimulus representations. Frontal and parietal ROIs displayed a qualitatively distinct, more "source-like" profile, wherein MVPA evidence for only the attended stimulus could be observed above baseline levels. To assess how attentional modulation of ventral occipito-temporal representations might relate to signals originating in the frontal and/or parietal ROIs, we analyzed informational connectivity (IC), which indexes time-varying covariation between regional levels of MVPA evidence. Parietal-posterior IC was elevated during the task, but did not differ for cued versus uncued items. Frontal-posterior IC, in contrast, was sensitive to an item's priority status. Thus, although regions of frontal and parietal cortex act as sources of top-down attentional control, their precise functions likely differ.

Landmarks: A solution for spatial navigation and memory experiments in virtual reality.

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.

Parietal-Occipital Interactions Underlying Control- and Representation-Related Processes in Working Memory for Nonspatial Visual Features.

Although the manipulation of load is popular in visual working memory research, many studies confound general attentional demands with context binding by drawing memoranda from the same stimulus category. In this fMRI study of human observers (both sexes), we created high- versus low-binding conditions, while holding load constant, by comparing trials requiring memory for the direction of motion of one random dot kinematogram (RDK; 1M trials) versus for three RDKs (3M), or versus one RDK and two color patches (1M2C). Memory precision was highest for 1M trials and comparable for 3M and 1M2C trials. And although delay-period activity in occipital cortex did not differ between the three conditions, returning to baseline for all three, multivariate pattern analysis decoding of a remembered RDK from occipital cortex was also highest for 1M trials and comparable for 3M and 1M2C trials. Delay-period activity in intraparietal sulcus (IPS), although elevated for all three conditions, displayed more sensitivity to demands on context binding than to load per se. The 1M-to-3M increase in IPS signal predicted the 1M-to-3M declines in both behavioral and neural estimates of working memory precision. These effects strengthened along a caudal-to-rostral gradient, from IPS0 to IPS5. Context binding-independent load sensitivity was observed when analyses were lateralized and extended into PFC, with trend-level effects evident in left IPS and strong effects in left lateral PFC. These findings illustrate how visual working memory capacity limitations arise from multiple factors that each recruit dissociable brain systems.SIGNIFICANCE STATEMENT Visual working memory capacity predicts performance on a wide array of cognitive and real-world outcomes. At least two theoretically distinct factors are proposed to influence visual working memory capacity limitations: an amodal attentional resource that must be shared across remembered items; and the demands on context binding. We unconfounded these two factors by varying load with items drawn from the same stimulus category ("high demands on context binding") versus items drawn from different stimulus categories ("low demands on context binding"). The results provide evidence for the dissociability, and the neural bases, of these two theorized factors, and they specify that the functions of intraparietal sulcus may relate more strongly to the control of representations than to the general allocation of attention.

Interacting networks of brain regions underlie human spatial navigation: a review and novel synthesis of the literature.

Navigation is an inherently dynamic and multimodal process, making isolation of the unique cognitive components underlying it challenging. The assumptions of much of the literature on human spatial navigation are that 1) spatial navigation involves modality independent, discrete metric representations (i.e., egocentric vs. allocentric), 2) such representations can be further distilled to elemental cognitive processes, and 3) these cognitive processes can be ascribed to unique brain regions. We argue that modality-independent spatial representations, instead of providing exact metrics about our surrounding environment, more often involve heuristics for estimating spatial topology useful to the current task at hand. We also argue that egocentric (body centered) and allocentric (world centered) representations are better conceptualized as involving a continuum rather than as discrete. We propose a neural model to accommodate these ideas, arguing that such representations also involve a continuum of network interactions centered on retrosplenial and posterior parietal cortex, respectively. Our model thus helps explain both behavioral and neural findings otherwise difficult to account for with classic models of spatial navigation and memory, providing a testable framework for novel experiments.

The short- and long-term fates of memory items retained outside the focus of attention.

When a test of working memory (WM) requires the retention of multiple items, a subset of them can be prioritized. Recent studies have shown that, although prioritized (i.e., attended) items are associated with active neural representations, unprioritized (i.e., unattended) memory items can be retained in WM despite the absence of such active representations, and with no decrement in their recognition if they are cued later in the trial. These findings raise two intriguing questions about the nature of the short-term retention of information outside the focus of attention. First, when the focus of attention shifts from items in WM, is there a loss of fidelity for those unattended memory items? Second, could the retention of unattended memory items be accomplished by long-term memory mechanisms? We addressed the first question by comparing the precision of recall of attended versus unattended memory items, and found a significant decrease in precision for unattended memory items, reflecting a degradation in the quality of those representations. We addressed the second question by asking subjects to perform a WM task, followed by a surprise memory test for the items that they had seen in the WM task. Long-term memory for unattended memory items from the WM task was not better than memory for items that had remained selected by the focus of attention in the WM task. These results show that unattended WM representations are degraded in quality and are not preferentially represented in long-term memory, as compared to attended memory items.

Rethinking retrosplenial cortex: Perspectives and predictions.

The last decade has produced exciting new ideas about retrosplenial cortex (RSC) and its role in integrating diverse inputs. Here, we review the diversity in forms of spatial and directional tuning of RSC activity, temporal organization of RSC activity, and features of RSC interconnectivity with other brain structures. We find that RSC anatomy and dynamics are more consistent with roles in multiple sensorimotor and cognitive processes than with any isolated function. However, two more generalized categories of function may best characterize roles for RSC in complex cognitive processes: (1) shifting and relating perspectives for spatial cognition and (2) prediction and error correction for current sensory states with internal representations of the environment. Both functions likely take advantage of RSC's capacity to encode conjunctions among sensory, motor, and spatial mapping information streams. Together, these functions provide the scaffold for intelligent actions, such as navigation, perspective taking, interaction with others, and error detection.

Wireless platform for controlled nitric oxide releasing optical fibers for mediating biological response to implanted devices.

Despite the documented potential to leverage nitric oxide generation to improve in vivo performance of implanted devices, a key limitation to current NO releasing materials tested thus far is that there has not been a means to modulate the level of NO release after it has been initiated. We report the fabrication of a wireless platform that uses light to release NO from a polymethylmethacrylate (PMMA) optical fiber coated with an S-nitroso-N-acetylpenicillamine derivatized polydimethylsiloxane (SNAP-PDMS). We demonstrate that a VAOL-5GSBY4 LED (λ(dominant)=460 nm) can be used as a dynamic trigger to vary the level of NO released from 500 µm diameter coated PMMA. The ability to generate programmable sequences of NO flux from the surface of these coated fibers offers precise spatial and temporal control over NO release and provides a platform to begin the systematic study of in vivo physiological response to implanted devices. NO surface fluxes up to 3.88 ± 0.57 × 10(-10)mol cm(-2)min(-1) were achieved with -100 µm thick coatings on the fibers and NO flux was pulsed, ramped and held steady using the wireless platform developed. We demonstrate the NO release is linearly proportional to the drive current applied to the LED (and therefore level of light produced from the LED). This system allow the surface flux of NO from the fibers to be continuously changed, providing a means to determine the level and duration of NO needed to mediate physiological response to blood contacting and subcutaneous implants and will ultimately lead to the intelligent design of NO releasing materials tailored to specific patterns of NO release needed to achieve reliable in vivo performance for intravascular and subcutaneous sensors and potentially for a wide variety of other implanted biomedical devices.

How Much of What We Learn in Virtual Reality Transfers to Real-World Navigation?

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.

Learning-dependent evolution of spatial representations in large-scale virtual environments.

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).

Perspective: Assessing the Flexible Acquisition, Integration, and Deployment of Human Spatial Representations and Information.

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 in vivo navigation, with some caveats.

Dissociation of frontal-midline delta-theta and posterior alpha oscillations: A mobile EEG study.

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.

Reactivation of latent working memories with transcranial magnetic stimulation.

The ability to hold information in working memory is fundamental for cognition. Contrary to the long-standing view that working memory depends on sustained, elevated activity, we present evidence suggesting that humans can hold information in working memory via "activity-silent" synaptic mechanisms. Using multivariate pattern analyses to decode brain activity patterns, we found that the active representation of an item in working memory drops to baseline when attention shifts away. A targeted pulse of transcranial magnetic stimulation produced a brief reemergence of the item in concurrently measured brain activity. This reactivation effect occurred and influenced memory performance only when the item was potentially relevant later in the trial, which suggests that the representation is dynamic and modifiable via cognitive control. The results support a synaptic theory of working memory.