Linking global top-down views to first-person views in the brain.

Humans and other animals have a remarkable capacity to translate their position from one spatial frame of reference to another. The ability to seamlessly move between top-down and first-person views is important for navigation, memory formation, and other cognitive tasks. Evidence suggests that the medial temporal lobe and other cortical regions contribute to this function. To understand how a neural system might carry out these computations, we used variational autoencoders (VAEs) to reconstruct the first-person view from the top-down view of a robot simulation, and vice versa. Many latent variables in the VAEs had similar responses to those seen in neuron recordings, including location-specific activity, head direction tuning, and encoding of distance to local objects. Place-specific responses were prominent when reconstructing a first-person view from a top-down view, but head direction-specific responses were prominent when reconstructing a top-down view from a first-person view. In both cases, the model could recover from perturbations without retraining, but rather through remapping. These results could advance our understanding of how brain regions support viewpoint linkages and transformations.

Theta oscillations support active exploration in human spatial navigation.

Active navigation seems to yield better spatial knowledge than passive navigation, but it is unclear how active decision-making influences learning and memory. Here, we examined the contributions of theta oscillations to memory-related exploration while testing theories about how they contribute to active learning. Using electroencephalography (EEG), we tested individuals on a maze-learning task in which they made discrete decisions about where to explore at each choice point in the maze. Half the participants were free to make active decisions at each choice point, and the other half passively explored by selecting a marked choice (matched to active exploration) at each intersection. Critically, all decisions were made when stationary, decoupling the active decision-making process from movement and speed factors, which is another prominent potential role for theta oscillations. Participants were then tested on their knowledge of the maze by traveling from object A to object B within the maze. Results show an advantage for active decision-making during learning and indicate that the active group had greater theta power during choice points in exploration, particularly in midfrontal channels. These findings demonstrate that active exploration is associated with theta oscillations during human spatial navigation, and that these oscillations are not exclusively related to movement or speed. Results demonstrating increased theta oscillations in prefrontal regions suggest communication with the hippocampus and integration of new information into memory. We also found evidence for alpha oscillations during active navigation, suggesting a role for attention as well. This study finds support for a general mnemonic role for theta oscillations during navigational learning.

Age-Related Changes in Spatial Navigation Are Evident by Midlife and Differ by Sex.

Accumulating evidence suggests that distinct aspects of successful navigation-path integration, spatial-knowledge acquisition, and navigation strategies-change with advanced age. Yet few studies have established whether navigation deficits emerge early in the aging process (prior to age 65) or whether early age-related deficits vary by sex. Here, we probed healthy young adults (ages 18-28) and midlife adults (ages 43-61) on three essential aspects of navigation. We found, first, that path-integration ability shows negligible effects of sex or age. Second, robust sex differences in spatial-knowledge acquisition are observed not only in young adulthood but also, although with diminished effect, at midlife. Third, by midlife, men and women show decreased ability to acquire spatial knowledge and increased reliance on taking habitual paths. Together, our findings indicate that age-related changes in navigation ability and strategy are evident as early as midlife and that path-integration ability is spared, to some extent, in the transition from youth to middle age.

Rotational error in path integration: encoding and execution errors in angle reproduction.

Path integration is fundamental to human navigation. When a navigator leaves home on a complex outbound path, they are able to keep track of their approximate position and orientation and return to their starting location on a direct homebound path. However, there are several sources of error during path integration. Previous research has focused almost exclusively on encoding error-the error in registering the outbound path in memory. Here, we also consider execution error-the error in the response, such as turning and walking a homebound trajectory. In two experiments conducted in ambulatory virtual environments, we examined the contribution of execution error to the rotational component of path integration using angle reproduction tasks. In the reproduction tasks, participants rotated once and then rotated again to face the original direction, either reproducing the initial turn or turning through the supplementary angle. One outstanding difficulty in disentangling encoding and execution error during a typical angle reproduction task is that as the encoding angle increases, so does the required response angle. In Experiment 1, we dissociated these two variables by asking participants to report each encoding angle using two different responses: by turning to walk on a path parallel to the initial facing direction in the same (reproduction) or opposite (supplementary angle) direction. In Experiment 2, participants reported the encoding angle by turning both rightward and leftward onto a path parallel to the initial facing direction, over a larger range of angles. The results suggest that execution error, not encoding error, is the predominant source of error in angular path integration. These findings also imply that the path integrator uses an intrinsic (action-scaled) rather than an extrinsic (objective) metric.

There and Back Again: Hippocampus and Retrosplenial Cortex Track Homing Distance during Human Path Integration.

Path integration, the updating of position and orientation during movement, often involves tracking a home location. Here, we examine processes that could contribute to successful location tracking in humans. In particular, we investigate a homing vector model of path integration, whereby a navigator continuously tracks a trajectory back to the home location. To examine this model, we developed a loop task for fMRI, in which participants viewed movement that circled back to a home location in a sparse virtual environment. In support of a homing vector system, hippocampus, retrosplenial cortex, and parahippocampal cortex were responsive to Euclidean distance from home. These results provide the first evidence of a constantly maintained homing signal in the human brain. In addition, hippocampus, retrosplenial cortex, and parahippocampal cortex, as well as medial prefrontal cortex, were recruited during successful path integration. These findings suggest that dynamic processes recruit hippocampus, retrosplenial cortex, and parahippocampal cortex in support of path integration, including a homing vector system that tracks movement relative to home. SIGNIFICANCE STATEMENT: Path integration is the continual updating of position and orientation during navigation. Animal studies have identified place cells and grid cells as important for path integration, but underlying models of path integration in humans have rarely been studied. The results of our novel loop closure task are the first to suggest that a homing vector tracks Euclidean distance from the home location, supported by the hippocampus, retrosplenial cortex, and parahippocampal cortex. These findings suggest a potential homing vector mechanism supporting path integration, which recruits hippocampus and retrosplenial cortex to track movement relative to home. These results provide new avenues for computational and animal models by directing attention to homing vector models of path integration, which differ from current movement-tracking models.

Which way and how far? Tracking of translation and rotation information for human path integration.

Path integration, the constant updating of the navigator's knowledge of position and orientation during movement, requires both visuospatial knowledge and memory. This study aimed to develop a systems-level understanding of human path integration by examining the basic building blocks of path integration in humans. To achieve this goal, we used functional imaging to examine the neural mechanisms that support the tracking and memory of translational and rotational components of human path integration. Critically, and in contrast to previous studies, we examined movement in translation and rotation tasks with no defined end-point or goal. Navigators accumulated translational and rotational information during virtual self-motion. Activity in hippocampus, retrosplenial cortex (RSC), and parahippocampal cortex (PHC) increased during both translation and rotation encoding, suggesting that these regions track self-motion information during path integration. These results address current questions regarding distance coding in the human brain. By implementing a modified delayed match to sample paradigm, we also examined the encoding and maintenance of path integration signals in working memory. Hippocampus, PHC, and RSC were recruited during successful encoding and maintenance of path integration information, with RSC selective for tasks that required processing heading rotation changes. These data indicate distinct working memory mechanisms for translation and rotation, which are essential for updating neural representations of current location. The results provide evidence that hippocampus, PHC, and RSC flexibly track task-relevant translation and rotation signals for path integration and could form the hub of a more distributed network supporting spatial navigation. Hum Brain Mapp 37:3636-3655, 2016. © 2016 Wiley Periodicals, Inc.

Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation.

Recent computational models suggest that visual input from optic flow provides information about egocentric (navigator-centered) motion and influences firing patterns in spatially tuned cells during navigation. Computationally, self-motion cues can be extracted from optic flow during navigation. Despite the importance of optic flow to navigation, a functional link between brain regions sensitive to optic flow and brain regions important for navigation has not been established in either humans or animals. Here, we used a beta-series correlation methodology coupled with two fMRI tasks to establish this functional link during goal-directed navigation in humans. Functionally defined optic flow sensitive cortical areas V3A, V6, and hMT+ were used as seed regions. fMRI data was collected during a navigation task in which participants updated position and orientation based on self-motion cues to successfully navigate to an encoded goal location. The results demonstrate that goal-directed navigation requiring updating of position and orientation in the first person perspective involves a cooperative interaction between optic flow sensitive regions V3A, V6, and hMT+ and the hippocampus, retrosplenial cortex, posterior parietal cortex, and medial prefrontal cortex. These functional connections suggest a dynamic interaction between these systems to support goal-directed navigation.

(Don't) look where you are going: Evidence for a travel direction signal in humans that is independent of head direction.

We often assume that travel direction is redundant with head direction, but from first principles, these two factors provide differing spatial information. Although head direction has been found to be a fundamental component of human navigation, it is unclear how self-motion signals for travel direction contribute to forming a travel trajectory. Employing a novel motion adaptation paradigm from visual neuroscience designed to preclude a contribution of head direction, we found high-level aftereffects of perceived travel direction, indicating that travel direction is a fundamental component of human navigation. Interestingly, we discovered a higher frequency of reporting perceived travel toward the adapted direction compared to a no-adapt control-an aftereffect that runs contrary to low-level motion aftereffects. This travel aftereffect was maintained after controlling for possible response biases and approaching effects, and it scaled with adaptation duration. These findings demonstrate the first evidence of how a pure travel direction signal might be represented in humans, independent of head direction. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Less spatial exploration is associated with poorer spatial memory in midlife adults.

Introduction: Despite its importance for navigation, very little is known about how the normal aging process affects spatial exploration behavior. We aimed to investigate: (1) how spatial exploration behavior may be altered early in the aging process, (2) the relationship between exploration behavior and subsequent spatial memory, and (3) whether exploration behavior can classify participants according to age. Methods: Fifty healthy young (aged 18-28) and 87 healthy midlife adults (aged 43-61) freely explored a desktop virtual maze, learning the locations of nine target objects. Various exploration behaviors (object visits, distance traveled, turns made, etc.) were measured. In the test phase, participants navigated from one target object to another without feedback, and their wayfinding success (% correct trials) was measured. Results: In the exploration phase, midlife adults exhibited less exploration overall compared to young adults, and prioritized learning target object locations over maze layout. In the test phase, midlife adults exhibited less wayfinding success when compared to the young adults. Furthermore, following principal components analysis (PCA), regression analyses indicated that both exploration quantity and quality components were associated with wayfinding success in the midlife group, but not the young adults. Finally, we could classify participants according to age with similar accuracy using either their exploration behavior or wayfinding success scores. Discussion: Our results aid in the understanding of how aging impacts spatial exploration, and encourages future investigations into how pathological aging may affect spatial exploration behavior.

Neuroanatomical changes observed over the course of a human pregnancy.

Pregnancy is a period of profound hormonal and physiological change experienced by millions of women annually, yet the neural changes unfolding in the maternal brain throughout gestation have not been studied in humans. Leveraging precision imaging, we mapped neuroanatomical changes in an individual from preconception through two years postpartum. Pronounced decreases in gray matter volume and cortical thickness were evident across the brain, which stand in contrast to increases in white matter microstructural integrity, ventricle volume, and cerebrospinal fluid, with few regions untouched by the transition to motherhood. This dataset serves as the first comprehensive map of the human brain across gestation, providing an open-access resource for the brain imaging community to stimulate further exploration and discovery.

Understanding Differences in Wayfinding Strategies.

Navigating to goal locations in a known environment (wayfinding) can be accomplished by different strategies, notably by taking habitual, well-learned routes (response strategy) or by inferring novel paths, such as shortcuts, from spatial knowledge of the environment's layout (place strategy). Human and animal neuroscience studies reveal that these strategies reflect different brain systems, with response strategies relying more on activation of the striatum and place strategies associated with activation of the hippocampus. In addition to individual differences in strategy, recent behavioral studies show sex differences such that men use place strategies more than women, and age differences such that older adults use more response strategies than younger adults. This paper takes a comprehensive multilevel approach to understanding these differences, characterizing wayfinding as a complex information processing task. This analysis reveals factors that affect navigation strategy, including availability of the relevant type of environmental knowledge, momentary access to this knowledge, trade-offs between physical and mental effort in different navigation contexts, and risk taking. We consider how strategies are influenced by the computational demands of a navigation task and by factors that affect the neural circuits underlying navigation. We also discuss limitations of laboratory studies to date and outline priorities for future research, including relating wayfinding strategies to independent measures of spatial knowledge, and studying wayfinding strategies in naturalistic environments.

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.

Directionality eclipses agency: How both directional and social cues improve spatial perspective taking.

Research on spatial perspective taking has suggested that including an agent in the display benefits performance. However, little research has examined the mechanisms underlying this benefit. Here, we examine how an agent benefits performance by examining its effects on three mental steps in a perspective-taking task: (1) imagining oneself at a location (station point) within in the array, (2) adopting a different perspective (heading), and (3) pointing to an object from that perspective. We also examine whether a non-agentive directional cue (an arrow) is sufficient to improve performance in an abstract map-like display. We compared a non-directional cue to two cues for position and orientation: a human figure (agentive, directional) and an arrow (non-agentive, directional). To examine the effects of cues on steps 2 and 3 of the perspective-taking process, magnitude of the initial perspective shift and pointing direction were varied across trials. Response time and error increased with the magnitude of the imagined perspective shift and pointing to the front was more accurate than pointing to the side, or back, but these effects were independent of directional cue. A directional cue alone was sufficient to improve performance relative to control, and agency did not provide additional benefit. The results overall indicate that most people adopt an embodied cognition strategy to perform this task and directional cues facilitate the first step of the perspective-taking process, imagining oneself at a location within in the array.

Executing the homebound path is a major source of error in homing by path integration.

Path integration-the constant updating of position and orientation in an environment-is an important component of spatial navigation, however, its mechanisms are poorly understood. The aims of this study are (a) to test the encoding-error model of path integration, which focuses solely on encoding as a potential source of error, and (b) to develop a model of path integration that best predicts path integration errors. We tested the encoding-error model by independently measuring participants' encoding errors in distance and angle reproduction tasks, and then using those reproduction errors to predict individual participants' errors in a triangle completion task. We sampled the distribution of encoding errors using Monte Carlo methods to predict the homebound path, and then compared the predictions to observed triangle completion behavior. The correlation between predicted errors and actual errors in the triangle completion task was extremely weak, whereas an alternative model using execution error alone was sufficient to describe the observed errors. A model incorporating both encoding and execution errors best described the triangle completion errors. These results suggest that errors in executing the response may contribute more to overall errors in path integration than do encoding errors, challenging the assumption that errors reflect encoding alone. Errors in triangle completion might not arise from failing to know where you are, but from an inability to get back home. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Telling right from right: the influence of handedness in the mental rotation of hands.

BACKGROUND: This study investigated the impact of handedness on a common spatial abilities task, the mental rotation task (MRT). The influence of a right-handed world was contrasted with people's embodied experience with their own hands by testing both left- and right-handed people on an MRT of right- and left-hand stimuli. An additional consideration is the influence of matching the shape of the hand stimuli with the proprioception of one's own hands. Two orthogonal hypothesis axes were crossed to yield four competing hypotheses. One axis contrasted (i) embodied experience versus (ii) world knowledge; the other axis contrasted (a) the match between the visual image of a hand on the screen and one's own hand versus (b) the resemblance of the shape outline information from the hand stimuli with the proprioception of one's own hands. RESULTS: Among people with mixed handedness, right-handers performed more accurately for left-hand stimuli, while left-handers had a trend for higher accuracy for right-hand stimuli. For people with extreme handedness, right-handers outperformed left-handers. Regardless of group, there was no significant variation in performance for left-hand stimuli, with only right-hand stimuli producing significant variation. CONCLUSIONS: No hypothesis fully aligned with all the data. For left-hand stimuli, the consistent performance across groups does not provide support for embodied experience, while world knowledge might influence all groups similarly. Alternatively, the within-group variation for mixed-handed people supports embodied experience in the hand MRT, likely processed through visual-proprioceptive integration.

Vision and proprioception make equal contributions to path integration in a novel homing task.

Navigation is a vital cognitive function for animals to find resources and avoid danger, and navigational processes are theorized to be a critical evolutionary foundation of episodic memory. Path integration, the continuous updating of position and orientation during self-motion, is a major contributor to spatial navigation. However, the most common paradigm for testing path integration-triangle completion-includes potential sources of error that cannot be disentangled. Here, we introduce a novel loop closure paradigm to test path integration, including the relative contributions of visual and body-based cues to performance. Contrary to triangle completion, we found that vestibular information alone led to chance performance, while visual optic flow and proprioception made relatively equal and independent contributions. The integration of these two cues was previously unknown, and we found that the two cues were not integrated in a Bayesian ideal manner. Our novel paradigm demonstrates the importance of both vision and proprioception to human path integration and provides the first test of optic flow and proprioception Bayesian cue combination for homing behavior. These findings open up new avenues to study navigation.

Heterogeneity in human retrosplenial cortex: A review of function and connectivity.

Retrosplenial cortex (RSC) is an important information hub in the brain and several mental disorders demonstrate RSC dysfunction, but its role is still largely unclear. Although researchers in many cognitive domains have recognized the importance of RSC, a broader synthesis of RSC function across cognitive domains is lacking. This review examines human RSC function across several cognitive domains, considering both specific cognitive functions and the RSC subregions in which that function occurs. Overall, this review found evidence for a functional gradient across the anterior-posterior axis of RSC involving several cognitive domains. Within the cognitive realm of navigation, RSC is important for path integration (including head direction), landmark processing, and the transformation between viewpoints. The related cognitive domain of scene processing encompasses information about place recognition and spatial context. Both navigation and scene processing are localized to more posterior subregions of RSC. Episodic memory (particularly episodic recall), mental imagery, and self-referential processing tend to be supported by anterior portions of RSC. The heterogeneity of RSC function is consistent with RSC anatomy and connectivity found in animal models. Finally, this review examines several common themes that emerged, including mental imagery and self-referential processing. Both the functional heterogeneity and the common themes of RSC function could provide new avenues for research and insight into the numerous mental disorders characterized by RSC dysfunction. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Resting State Connectivity Between Medial Temporal Lobe Regions and Intrinsic Cortical Networks Predicts Performance in a Path Integration Task.

Humans differ in their individual navigational performance, in part because successful navigation relies on several diverse abilities. One such navigational capability is path integration, the updating of position and orientation during movement, typically in a sparse, landmark-free environment. This study examined the relationship between path integration abilities and functional connectivity to several canonical intrinsic brain networks. Intrinsic networks within the brain reflect past inputs and communication as well as structural architecture. Individual differences in intrinsic connectivity have been observed for common networks, suggesting that these networks can inform our understanding of individual spatial abilities. Here, we examined individual differences in intrinsic connectivity using resting state magnetic resonance imaging (rsMRI). We tested path integration ability using a loop closure task, in which participants viewed a single video of movement in a circle trajectory in a sparse environment, and then indicated whether the video ended in the same location in which it started. To examine intrinsic brain networks, participants underwent a resting state scan. We found that better performance in the loop task was associated with increased connectivity during rest between the central executive network (CEN) and posterior hippocampus, parahippocampal cortex (PHC) and entorhinal cortex. We also found that connectivity between PHC and the default mode network (DMN) during rest was associated with better loop closure performance. The results indicate that interactions between medial temporal lobe (MTL) regions and intrinsic networks that involve prefrontal cortex (PFC) are important for path integration and navigation.

Converging meta-analytic and connectomic evidence for functional subregions within the human retrosplenial region.

Interest in the retrosplenial cortex (RSC) has surged in recent years, as this region has been implicated in a range of cognitive processes. Previously reported anatomical and functional definitions of the human RSC encompass a larger area than expected from underlying cytoarchitectonic profiles. Here, we used a large-scale, unbiased, and data-driven approach combining functional MRI meta-analysis and resting-state functional connectivity (rsFC) methods to test the nature of this heterogeneity. The automated toolset Neurosynth was used to conduct meta-analyses in order to (a) identify heterogeneous areas in the retrosplenial region (RS region) associated with one or more cognitive domains, and (b) contrast the activation profiles related to these domains. These analyses yielded several functional subregions across the RS region, highlighting differences between anterior RS regions associated with episodic memory and posterior RS regions in the parietal-occipital sulcus associated with scenes and navigation. These regions were subsequently used as seeds to conduct whole brain rsFC analyses using data from the Human Connectome Project. In support of the meta-analysis findings, rsFC revealed divergent connectivity profiles, with anterior regions demonstrating connectivity to the default mode network (DMN) and posterior regions demonstrating connectivity to visual regions. Anterior RS regions and the parietal-occipital sulcus connected to different subnetworks of the DMN. This convergent evidence supports the conclusion that the broad cortical RS region incorporating both anatomical and functional RSC consists of functionally heterogeneous subregions. This study combines two large databases to provide a novel methodological blueprint for understanding brain function in the RS region and beyond. (PsycINFO Database Record (c) 2018 APA, all rights reserved).