From cognitive maps to spatial schemas.

A schema refers to a structured body of prior knowledge that captures common patterns across related experiences. Schemas have been studied separately in the realms of episodic memory and spatial navigation across different species and have been grounded in theories of memory consolidation, but there has been little attempt to integrate our understanding across domains, particularly in humans. We propose that experiences during navigation with many similarly structured environments give rise to the formation of spatial schemas (for example, the expected layout of modern cities) that share properties with but are distinct from cognitive maps (for example, the memory of a modern city) and event schemas (such as expected events in a modern city) at both cognitive and neural levels. We describe earlier theoretical frameworks and empirical findings relevant to spatial schemas, along with more targeted investigations of spatial schemas in human and non-human animals. Consideration of architecture and urban analytics, including the influence of scale and regionalization, on different properties of spatial schemas may provide a powerful approach to advance our understanding of spatial schemas.

A neural circuit for spatial orientation derived from brain lesions.

There is disagreement regarding the major components of the brain network supporting spatial cognition. To address this issue, we applied a lesion mapping approach to the clinical phenomenon of topographical disorientation. Topographical disorientation is the inability to maintain accurate knowledge about the physical environment and use it for navigation. A review of published topographical disorientation cases identified 65 different lesion sites. Our lesion mapping analysis yielded a topographical disorientation brain map encompassing the classic regions of the navigation network: medial parietal, medial temporal, and temporo-parietal cortices. We also identified a ventromedial region of the prefrontal cortex, which has been absent from prior descriptions of this network. Moreover, we revealed that the regions mapped are correlated with the Default Mode Network sub-network C. Taken together, this study provides causal evidence for the distribution of the spatial cognitive system, demarking the major components and identifying novel regions.

Humans account for cognitive costs when finding shortcuts: An information-theoretic analysis of navigation.

When faced with navigating back somewhere we have been before we might either retrace our steps or seek a shorter path. Both choices have costs. Here, we ask whether it is possible to characterize formally the choice of navigational plans as a bounded rational process that trades off the quality of the plan (e.g., its length) and the cognitive cost required to find and implement it. We analyze the navigation strategies of two groups of people that are firstly trained to follow a "default policy" taking a route in a virtual maze and then asked to navigate to various known goal destinations, either in the way they want ("Go To Goal") or by taking novel shortcuts ("Take Shortcut"). We address these wayfinding problems using InfoRL: an information-theoretic approach that formalizes the cognitive cost of devising a navigational plan, as the informational cost to deviate from a well-learned route (the "default policy"). In InfoRL, optimality refers to finding the best trade-off between route length and the amount of control information required to find it. We report five main findings. First, the navigational strategies automatically identified by InfoRL correspond closely to different routes (optimal or suboptimal) in the virtual reality map, which were annotated by hand in previous research. Second, people deliberate more in places where the value of investing cognitive resources (i.e., relevant goal information) is greater. Third, compared to the group of people who receive the "Go To Goal" instruction, those who receive the "Take Shortcut" instruction find shorter but less optimal solutions, reflecting the intrinsic difficulty of finding optimal shortcuts. Fourth, those who receive the "Go To Goal" instruction modulate flexibly their cognitive resources, depending on the benefits of finding the shortcut. Finally, we found a surprising amount of variability in the choice of navigational strategies and resource investment across participants. Taken together, these results illustrate the benefits of using InfoRL to address navigational planning problems from a bounded rational perspective.

Landmark-dependent Navigation Strategy Declines across the Human Life-Span: Evidence from Over 37,000 Participants.

Humans show a remarkable capacity to navigate various environments using different navigation strategies, and we know that strategy changes across the life span. However, this observation has been based on studies of small sample sizes. To this end, we used a mobile app-based video game (Sea Hero Quest) to test virtual navigation strategies and memory performance within a distinct radial arm maze level in over 37,000 participants. Players were presented with six pathways (three open and three closed) and were required to navigate to the three open pathways to collect a target. Next, all six pathways were made available and the player was required to visit the pathways that were previously unavailable. Both reference memory and working memory errors were calculated. Crucially, at the end of the level, the player was asked a multiple-choice question about how they found the targets (i.e., a counting-dependent strategy vs. a landmark-dependent strategy). As predicted from previous laboratory studies, we found the use of landmarks declined linearly with age. Those using landmark-based strategies also performed better on reference memory than those using a counting-based strategy. These results extend previous observations in the laboratory showing a decreased use of landmark-dependent strategies with age.

Examining individual learning patterns using generalised linear mixed models.

Everyone learns differently, but individual performance is often ignored in favour of a group-level analysis. Using data from four different experiments, we show that generalised linear mixed models (GLMMs) and extensions can be used to examine individual learning patterns. Producing ellipsoids and cluster analyses based on predicted random effects, individual learning patterns can be identified, clustered and used for comparisons across various experimental conditions or groups. This analysis can handle a range of datasets including discrete, continuous, censored and non-censored, as well as different experimental conditions, sample sizes and trial numbers. Using this approach, we show that learning a face-named paired associative task produced individuals that can learn quickly, with the performance of some remaining high, but with a drop-off in others, whereas other individuals show poor performance throughout the learning period. We see this more clearly in a virtual navigation spatial learning task (NavWell). Two prominent clusters of learning emerged, one showing individuals who produced a rapid learning and another showing a slow and gradual learning pattern. Using data from another spatial learning task (Sea Hero Quest), we show that individuals' performance generally reflects their age category, but not always. Overall, using this analytical approach may help practitioners in education and medicine to identify those individuals who might need extra help and attention. In addition, identifying learning patterns may enable further investigation of the underlying neural, biological, environmental and other factors associated with these individuals.

London taxi drivers: A review of neurocognitive studies and an exploration of how they build their cognitive map of London.

Licensed London taxi drivers have been found to show changes in the gray matter density of their hippocampus over the course of training and decades of navigation in London (UK). This has been linked to their learning and using of the "Knowledge of London," the names and layout of over 26,000 streets and thousands of points of interest in London. Here we review past behavioral and neuroimaging studies of London taxi drivers, covering the structural differences in hippocampal gray matter density and brain dynamics associated with navigating London. We examine the process by which they learn the layout of London, detailing the key learning steps: systematic study of maps, travel on selected overlapping routes, the mental visualization of places and the optimal use of subgoals. Our analysis provides the first map of the street network covered by the routes used to learn the network, allowing insight into where there are gaps in this network. The methods described could be widely applied to aid spatial learning in the general population and may provide insights for artificial intelligence systems to efficiently learn new environments.

Toward personalized cognitive diagnostics of at-genetic-risk Alzheimer's disease.

Spatial navigation is emerging as a critical factor in identifying preclinical Alzheimer's disease (AD). However, the impact of interindividual navigation ability and demographic risk factors (e.g., APOE, age, and sex) on spatial navigation make it difficult to identify persons "at high risk" of AD in the preclinical stages. In the current study, we use spatial navigation big data (n = 27,108) from the Sea Hero Quest (SHQ) game to overcome these challenges by investigating whether big data can be used to benchmark a highly phenotyped healthy aging laboratory cohort into high- vs. low-risk persons based on their genetic (APOE) and demographic (sex, age, and educational attainment) risk factors. Our results replicate previous findings in APOE ε4 carriers, indicative of grid cell coding errors in the entorhinal cortex, the initial brain region affected by AD pathophysiology. We also show that although baseline navigation ability differs between men and women, sex does not interact with the APOE genotype to influence the manifestation of AD-related spatial disturbance. Most importantly, we demonstrate that such high-risk preclinical cases can be reliably distinguished from low-risk participants using big-data spatial navigation benchmarks. By contrast, participants were undistinguishable on neuropsychological episodic memory tests. Taken together, we present evidence to suggest that, in the future, SHQ normative benchmark data can be used to more accurately classify spatial impairments in at-high-risk of AD healthy participants at a more individual level, therefore providing the steppingstone for individualized diagnostics and outcome measures of cognitive symptoms in preclinical AD.

Hippocampal and Retrosplenial Goal Distance Coding After Long-term Consolidation of a Real-World Environment.

Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (>2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the distance to the goal in the newly learned campus, as well as in familiar environments when the future route contained many turns. By contrast retrosplenial cortex only tracked the distance to the goal in the familiar campus. All of these responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and underscore the notion that the hippocampus continues to play a role in navigation when detailed processing of the environment is needed for navigation.

Prefrontal Dynamics Associated with Efficient Detours and Shortcuts: A Combined Functional Magnetic Resonance Imaging and Magnetoencenphalography Study.

Central to the concept of the "cognitive map" is that it confers behavioral flexibility, allowing animals to take efficient detours, exploit shortcuts, and avoid alluring, but unhelpful, paths. The neural underpinnings of such naturalistic and flexible behavior remain unclear. In two neuroimaging experiments, we tested human participants on their ability to navigate to a set of goal locations in a virtual desert island riven by lava, which occasionally spread to block selected paths (necessitating detours) or receded to open new paths (affording real shortcuts or false shortcuts to be avoided). Detours activated a network of frontal regions compared with shortcuts. Activity in the right dorsolateral PFC specifically increased when participants encountered tempting false shortcuts that led along suboptimal paths that needed to be differentiated from real shortcuts. We also report modulation in event-related fields and theta power in these situations, providing insight to the temporal evolution of response to encountering detours and shortcuts. These results help inform current models as to how the brain supports navigation and planning in dynamic environments.

Cognitive mapping style relates to posterior-anterior hippocampal volume ratio.

As London taxi drivers acquire "the knowledge" and develop a detailed cognitive map of London, their posterior hippocampi (pHPC) gradually increase in volume, reflecting an increasing pHPC/aHPC volume ratio. In the mnemonic domain, greater pHPC/aHPC volume ratios in young adults have been found to relate to better recollection ability, indicating that the balance between pHPC and aHPC volumes might be reflective of cross-domain individual differences. Here, we examined participants' self-reported use of cognitive map-based navigational strategies in relation to their pHPC/aHPC hippocampal volume ratio. We find that greater reported cognitive map use was related to significantly greater posterior, relative to anterior, hippocampal volume in two separate samples of young adults. Further, greater reported cognitive map usage correlated with better performance on a self-initiated navigation task. Together, these data help to advance our understanding of differences between aHPC and pHPC and the greater role of pHPC in spatial mapping.

Backtracking during navigation is correlated with enhanced anterior cingulate activity and suppression of alpha oscillations and the 'default-mode' network.

Successful navigation can require realizing the current path choice was a mistake and the best strategy is to retreat along the recent path: 'back-track'. Despite the wealth of studies on the neural correlates of navigation little is known about backtracking. To explore the neural underpinnings of backtracking we tested humans during functional magnetic resonance imaging on their ability to navigate to a set of goal locations in a virtual desert island riven by lava which constrained the paths that could be taken. We found that on a subset of trials, participants spontaneously chose to backtrack and that the majority of these choices were optimal. During backtracking, activity increased in frontal regions and the dorsal anterior cingulate cortex, while activity was suppressed in regions associated with the core default-mode network. Using the same task, magnetoencephalography and a separate group of participants, we found that power in the alpha band was significantly decreased immediately prior to such backtracking events. These results highlight the importance for navigation of brain networks previously identified in processing internally-generated errors and that such error-detection responses may involve shifting the brain from default-mode states to aid successful spatial orientation.

Semantic representations in the temporal pole predict false memories.

Recent advances in neuroscience have given us unprecedented insight into the neural mechanisms of false memory, showing that artificial memories can be inserted into the memory cells of the hippocampus in a way that is indistinguishable from true memories. However, this alone is not enough to explain how false memories can arise naturally in the course of our daily lives. Cognitive psychology has demonstrated that many instances of false memory, both in the laboratory and the real world, can be attributed to semantic interference. Whereas previous studies have found that a diverse set of regions show some involvement in semantic false memory, none have revealed the nature of the semantic representations underpinning the phenomenon. Here we use fMRI with representational similarity analysis to search for a neural code consistent with semantic false memory. We find clear evidence that false memories emerge from a similarity-based neural code in the temporal pole, a region that has been called the "semantic hub" of the brain. We further show that each individual has a partially unique semantic code within the temporal pole, and this unique code can predict idiosyncratic patterns of memory errors. Finally, we show that the same neural code can also predict variation in true-memory performance, consistent with an adaptive perspective on false memory. Taken together, our findings reveal the underlying structure of neural representations of semantic knowledge, and how this semantic structure can both enhance and distort our memories.

Oscillatory Reinstatement Enhances Declarative Memory.

Declarative memory recall is thought to involve the reinstatement of neural activity patterns that occurred previously during encoding. Consistent with this view, greater similarity between patterns of activity recorded during encoding and retrieval has been found to predict better memory performance in a number of studies. Recent models have argued that neural oscillations may be crucial to reinstatement for successful memory retrieval. However, to date, no causal evidence has been provided to support this theory, nor has the impact of oscillatory electrical brain stimulation during encoding and retrieval been assessed. To explore this we used transcranial alternating current stimulation over the left dorsolateral prefrontal cortex of human participants [n = 70, 45 females; age mean (SD) = 22.12 (2.16)] during a declarative memory task. Participants received either the same frequency during encoding and retrieval (60-60 or 90-90 Hz) or different frequencies (60-90 or 90-60 Hz). When frequencies matched there was a significant memory improvement (at both 60 and 90 Hz) relative to sham stimulation. No improvement occurred when frequencies mismatched. Our results provide support for the role of oscillatory reinstatement in memory retrieval.SIGNIFICANCE STATEMENT Recent neurobiological models of memory have argued that large-scale neural oscillations are reinstated to support successful memory retrieval. Here we used transcranial alternating current stimulation (tACS) to test these models. tACS has recently been shown to induce neural oscillations at the frequency stimulated. We stimulated over the left dorsolateral prefrontal cortex during a declarative memory task involving learning a set of words. We found that tACS applied at the same frequency during encoding and retrieval enhances memory. We also find no difference between the two applied frequencies. Thus our results are consistent with the proposal that reinstatement of neural oscillations during retrieval supports successful memory retrieval.

Hippocampal CA1 activity correlated with the distance to the goal and navigation performance.

Coding the distance to a future goal is an important function of a neural system supporting navigation. While some evidence indicates the hippocampus increases activity with proximity to the goal, others have found activity to decrease with proximity. To explore goal distance coding in the hippocampus we recorded from CA1 hippocampal place cells in rats as they navigated to learned goals in an event arena with a win-stay lose-shift rule. CA1 activity was positively correlated with the distance - decreasing with proximity to the goal. The stronger the correlation between distance to the goal and CA1 activity, the more successful navigation was in a given task session. Acceleration, but not speed, was also correlated with the distance to the goal. However, the relationship between CA1 activity and navigation performance was independent of variation in acceleration and variation in speed. These results help clarify the situations in which CA1 activity encodes navigationally relevant information and the extent to which it relates to behavior.

Anterior Temporal Lobe Tracks the Formation of Prejudice.

Despite advances in understanding the brain structures involved in the expression of stereotypes and prejudice, little is known about the brain structures involved in their acquisition. Here, we combined fMRI, a task involving learning the valence of different social groups, and modeling of the learning process involved in the development of biases in thinking about social groups that support prejudice. Participants read descriptions of valenced behaviors performed by members of novel social groups, with majority groups being more frequently encountered during learning than minority groups. A model-based fMRI analysis revealed that the anterior temporal lobe tracked the trial-by-trial changes in the valence associated with each group encountered in the task. Descriptions of behavior by group members that deviated from the group average (i.e., prediction errors) were associated with activity in the left lateral PFC, dorsomedial PFC, and lateral anterior temporal cortex. Minority social groups were associated with slower acquisition rates and more activity in the ventral striatum and ACC/dorsomedial PFC compared with majority groups. These findings provide new insights into the brain regions that (a) support the acquisition of prejudice and (b) detect situations in which an individual's behavior deviates from the prejudicial attitude held toward their group.

Familiarity expands space and contracts time.

When humans draw maps, or make judgments about travel-time, their responses are rarely accurate and are often systematically distorted. Distortion effects on estimating time to arrival and the scale of sketch-maps reveal the nature of mental representation of time and space. Inspired by data from rodent entorhinal grid cells, we predicted that familiarity to an environment would distort representations of the space by expanding the size of it. We also hypothesized that travel-time estimation would be distorted in the same direction as space-size, if time and space rely on the same cognitive map. We asked international students, who had lived at a college in London for 9 months, to sketch a south-up map of their college district, estimate travel-time to destinations within the area, and mark their everyday walking routes. We found that while estimates for sketched space were expanded with familiarity, estimates of the time to travel through the space were contracted with familiarity. Thus, we found dissociable responses to familiarity in representations of time and space. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.

Place field repetition and purely local remapping in a multicompartment environment.

Hippocampal place cells support spatial memory using sensory information from the environment and self-motion information to localize their firing fields. Currently, there is disagreement about whether CA1 place cells can use pure self-motion information to disambiguate different compartments in environments containing multiple visually identical compartments. Some studies report that place cells can disambiguate different compartments, while others report that they do not. Furthermore, while numerous studies have examined remapping, there has been little examination of remapping in different subregions of a single environment. Is remapping purely local or do place fields in neighboring, unaffected, regions detect the change? We recorded place cells as rats foraged across a 4-compartment environment and report 3 new findings. First, we find that, unlike studies in which rats foraged in 2 compartments, place fields showed a high degree of spatial repetition with a slight degree of rate-based discrimination. Second, this repetition does not diminish with extended experience. Third, remapping was found to be purely local for both geometric change and contextual change. Our results reveal the limited capacity of the path integrator to drive pattern separation in hippocampal representations, and suggest that doorways may play a privileged role in segmenting the neural representation of space.

Sleep enhances a spatially mediated generalization of learned values.

Sleep is thought to play an important role in memory consolidation. Here we tested whether sleep alters the subjective value associated with objects located in spatial clusters that were navigated to in a large-scale virtual town. We found that sleep enhances a generalization of the value of high-value objects to the value of locally clustered objects, resulting in an impaired memory for the value of high-valued objects. Our results are consistent with (a) spatial context helping to bind items together in long-term memory and serve as a basis for generalizing across memories and (b) sleep mediating memory effects on salient/reward-related items.

Transcranial electrical brain stimulation modulates neuronal tuning curves in perception of numerosity and duration.

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation method with many putative applications and reported to effectively modulate behaviour. However, its effects have yet to be considered at a computational level. To address this we modelled the tuning curves underlying the behavioural effects of stimulation in a perceptual task. Participants judged which of the two serially presented images contained more items (numerosity judgement task) or was presented longer (duration judgement task). During presentation of the second image their posterior parietal cortices (PPCs) were stimulated bilaterally with opposite polarities for 1.6s. We also examined the impact of three stimulation conditions on behaviour: anodal right-PPC and cathodal left-PPC (rA-lC), reverse order (lA-rC) and no-stimulation condition. Behavioural results showed that participants were more accurate in numerosity and duration judgement tasks when they were stimulated with lA-rC and rA-lC stimulation conditions respectively. Simultaneously, a decrease in performance on numerosity and duration judgement tasks was observed when the stimulation condition favoured the other task. Thus, our results revealed a double-dissociation of laterality and task. Importantly, we were able to model the effects of stimulation on behaviour. Our computational modelling showed that participants' superior performance was attributable to a narrower tuning curve--smaller standard deviation of detection noise. We believe that this approach may prove useful in understanding the impact of brain stimulation on other cognitive domains.