Spontaneous eye movements reflect the representational geometries of conceptual spaces.

Functional neuroimaging studies indicate that the human brain can represent concepts and their relational structure in memory using coding schemes typical of spatial navigation. However, whether we can read out the internal representational geometries of conceptual spaces solely from human behavior remains unclear. Here, we report that the relational structure between concepts in memory might be reflected in spontaneous eye movements during verbal fluency tasks: When we asked participants to randomly generate numbers, their eye movements correlated with distances along the left-to-right one-dimensional geometry of the number space (mental number line), while they scaled with distance along the ring-like two-dimensional geometry of the color space (color wheel) when they randomly generated color names. Moreover, when participants randomly produced animal names, eye movements correlated with low-dimensional similarity in word frequencies. These results suggest that the representational geometries used to internally organize conceptual spaces might be read out from gaze behavior.

Development and validation of a questionnaire for assessing visual and auditory spatial localization abilities in dual sensory impairment.

Spatial localization is important for social interaction and safe mobility, and relies heavily on vision and hearing. While people with vision or hearing impairment compensate with their intact sense, people with dual sensory impairment (DSI) may require rehabilitation strategies that take both impairments into account. There is currently no tool for assessing the joint effect of vision and hearing impairment on spatial localization in this large and increasing population. To this end, we developed a novel Dual Sensory Spatial Localization Questionnaire (DS-SLQ) that consists of 35 everyday spatial localization tasks. The DS-SLQ asks participants about their difficulty completing different tasks using only vision or hearing, as well as the primary sense they rely on for each task. We administered the DS-SLQ to 104 participants with heterogenous vision and hearing status. Rasch analysis confirmed the psychometric validity of the DS-SLQ and the feasibility of comparing vision and hearing spatial abilities in a unified framework. Vision and hearing impairment were associated with decreased visual and auditory spatial abilities. Differences between vision and hearing abilities predicted overall sensory reliance patterns. In DSI rehabilitation, DS-SLQ may be useful for measuring vision and hearing spatial localization abilities and predicting the better sense for completing different spatial localization tasks.

Analysis of hippocampal local field potentials by diffusion mapped delay coordinates.

Spatial navigation through novel spaces and to known goal locations recruits multiple integrated structures in the mammalian brain. Within this extended network, the hippocampus enables formation and retrieval of cognitive spatial maps and contributes to decision making at choice points. Exploration and navigation to known goal locations produce synchronous activity of hippocampal neurons resulting in rhythmic oscillation events in local networks. Power of specific oscillatory frequencies and numbers of these events recorded in local field potentials correlate with distinct cognitive aspects of spatial navigation. Typically, oscillatory power in brain circuits is analyzed with Fourier transforms or short-time Fourier methods, which involve assumptions about the signal that are likely not true and fail to succinctly capture potentially informative features. To avoid such assumptions, we applied a method that combines manifold discovery techniques with dynamical systems theory, namely diffusion maps and Takens' time-delay embedding theory, that avoids limitations seen in traditional methods. This method, called diffusion mapped delay coordinates (DMDC), when applied to hippocampal signals recorded from juvenile rats freely navigating a Y-maze, replicates some outcomes seen with standard approaches and identifies age differences in dynamic states that traditional analyses are unable to detect. Thus, DMDC may serve as a suitable complement to more traditional analyses of LFPs recorded from behaving subjects that may enhance information yield.

Individual differences in knowledge network navigation.

With the rapid accumulation of online information, efficient web navigation has grown vital yet challenging. To create an easily navigable cyberspace catering to diverse demographics, understanding how people navigate differently is paramount. While previous research has unveiled individual differences in spatial navigation, such differences in knowledge space navigation remain sparse. To bridge this gap, we conducted an online experiment where participants played a navigation game on Wikipedia and completed personal information questionnaires. Our analysis shows that age negatively affects knowledge space navigation performance, while multilingualism enhances it. Under time pressure, participants' performance improves across trials and males outperform females, an effect not observed in games without time pressure. In our experiment, successful route-finding is usually not related to abilities of innovative exploration of routes. Our results underline the importance of age, multilingualism and time constraint in the knowledge space navigation.

Conjunctive encoding of exploratory intentions and spatial information in the hippocampus.

The hippocampus creates a cognitive map of the external environment by encoding spatial and self-motion-related information. However, it is unclear whether hippocampal neurons could also incorporate internal cognitive states reflecting an animal's exploratory intention, which is not driven by rewards or unexpected sensory stimuli. In this study, a subgroup of CA1 neurons was found to encode both spatial information and animals' investigatory intentions in male mice. These neurons became active before the initiation of exploration behaviors at specific locations and were nearly silent when the same fields were traversed without exploration. Interestingly, this neuronal activity could not be explained by object features, rewards, or mismatches in environmental cues. Inhibition of the lateral entorhinal cortex decreased the activity of these cells during exploration. Our findings demonstrate that hippocampal neurons may bridge external and internal signals, indicating a potential connection between spatial representation and intentional states in the construction of internal navigation systems.

Altered grid-like coding in early blind people.

Cognitive maps in the hippocampal-entorhinal system are central for the representation of both spatial and non-spatial relationships. Although this system, especially in humans, heavily relies on vision, the role of visual experience in shaping the development of cognitive maps remains largely unknown. Here, we test sighted and early blind individuals in both imagined navigation in fMRI and real-world navigation. During imagined navigation, the Human Navigation Network, constituted by frontal, medial temporal, and parietal cortices, is reliably activated in both groups, showing resilience to visual deprivation. However, neural geometry analyses highlight crucial differences between groups. A 60° rotational symmetry, characteristic of a hexagonal grid-like coding, emerges in the entorhinal cortex of sighted but not blind people, who instead show a 90° (4-fold) symmetry, indicative of a square grid. Moreover, higher parietal cortex activity during navigation in blind people correlates with the magnitude of 4-fold symmetry. In sum, early blindness can alter the geometry of entorhinal cognitive maps, possibly as a consequence of higher reliance on parietal egocentric coding during navigation.

Changes in spatial self-consciousness elicit grid cell-like representation in the entorhinal cortex.

Grid cells in the entorhinal cortex (EC) encode an individual's location in space, integrating both environmental and multisensory bodily cues. Notably, body-derived signals are also primary signals for the sense of self. While studies have demonstrated that continuous application of visuo-tactile bodily stimuli can induce perceptual shifts in self-location, it remains unexplored whether these illusory changes suffice to trigger grid cell-like representation (GCLR) within the EC, and how this compares to GCLR during conventional virtual navigation. To address this, we systematically induced illusory drifts in self-location toward controlled directions using visuo-tactile bodily stimulation, while maintaining the subjects' visual viewpoint fixed (absent conventional virtual navigation). Subsequently, we evaluated the corresponding GCLR in the EC through functional MRI analysis. Our results reveal that illusory changes in perceived self-location (independent of changes in environmental navigation cues) can indeed evoke entorhinal GCLR, correlating in strength with the magnitude of perceived self-location, and characterized by similar grid orientation as during conventional virtual navigation in the same virtual room. These data demonstrate that the same grid-like representation is recruited when navigating based on environmental, mainly visual cues, or when experiencing illusory forward drifts in self-location, driven by perceptual multisensory bodily cues.

Stress affects navigation strategies in immersive virtual reality.

There are known individual differences in both the ability to learn the layout of novel environments and the flexibility of strategies for navigating known environments. However, it is unclear how navigational abilities are impacted by high-stress scenarios. Here we used immersive virtual reality (VR) to develop a novel behavioral paradigm to examine navigation under dynamically changing situations. We recruited 48 participants (24 female; ages 17-32) to navigate a virtual maze (7.5 m × 7.5 m). Participants learned the maze by moving along a fixed path past the maze's landmarks (paintings). Subsequently, participants experienced either a non-stress condition, or a high-stress condition tasking them with navigating the maze. In the high-stress condition, their initial path was blocked, the environment was darkened, threatening music was played, fog obstructed more distal views of the environment, and participants were given a time limit of 20 s with a countdown timer displayed at the top of their screen. On trials where the path was blocked, we found self-reported stress levels and distance traveled increased while trial completion rate decreased (as compared to non-stressed control trials). On unblocked stress trials, participants were less likely to take a shortcut and consequently navigated less efficiently compared to control trials. Participants with more trait spatial anxiety reported more stress and navigated less efficiently. Overall, our results suggest that navigational abilities change considerably under high-stress conditions.

Neonatal GABAergic transmission primes vestibular gating of output for adult spatial navigation.

GABAergic interneurons are poised with the capacity to shape circuit output via inhibitory gating. How early in the development of medial vestibular nucleus (MVN) are GABAergic neurons recruited for feedforward shaping of outputs to higher centers for spatial navigation? The role of early GABAergic transmission in assembling vestibular circuits for spatial navigation was explored by neonatal perturbation. Immunohistochemistry and confocal imaging were utilized to reveal the expression of parvalbumin (PV)-expressing MVN neurons and their perineuronal nets. Whole-cell patch-clamp recording, coupled with optogenetics, was conducted in vitro to examine the synaptic function of MVN circuitry. Chemogenetic targeting strategy was also employed in vivo to manipulate neuronal activity during navigational tests. We found in rats a neonatal critical period before postnatal day (P) 8 in which competitive antagonization of GABAergic transmission in the MVN retarded maturation of inhibitory neurotransmission, as evidenced by deranged developmental trajectory for excitation/inhibition ratio and an extended period of critical period-like plasticity in GABAergic transmission. Despite increased number of PV-expressing GABAergic interneurons in the MVN, optogenetic-coupled patch-clamp recording indicated null-recruitment of these neurons in tuning outputs along the ascending vestibular pathway. Such perturbation not only offset output dynamics of ascending MVN output neurons, but was further accompanied by impaired vestibular-dependent navigation in adulthood. The same perturbations were however non-consequential when applied after P8. Results highlight neonatal GABAergic transmission as key to establishing feedforward output dynamics to higher brain centers for spatial cognition and navigation.

Repetition Suppression Reveals Cue-Specific Spatial Representations for Landmarks and Self-Motion Cues in the Human Retrosplenial Cortex.

The efficient use of various spatial cues within a setting is crucial for successful navigation. Two fundamental forms of spatial navigation, landmark-based and self-motion-based, engage distinct cognitive mechanisms. The question of whether these modes invoke shared or separate spatial representations in the brain remains unresolved. While nonhuman animal studies have yielded inconsistent results, human investigation is limited. In our previous work (Chen et al., 2019), we introduced a novel spatial navigation paradigm utilizing ultra-high field fMRI to explore neural coding of positional information. We found that different entorhinal subregions in the right hemisphere encode positional information for landmarks and self-motion cues. The present study tested the generalizability of our previous finding with a modified navigation paradigm. Although we did not replicate our previous finding in the entorhinal cortex, we identified adaptation-based allocentric positional codes for both cue types in the retrosplenial cortex (RSC), which were not confounded by the path to the spatial location. Crucially, the multi-voxel patterns of these spatial codes differed between the cue types, suggesting cue-specific positional coding. The parahippocampal cortex exhibited positional coding for self-motion cues, which was not dissociable from path length. Finally, the brain regions involved in successful navigation differed from our previous study, indicating overall distinct neural mechanisms recruited in our two studies. Taken together, the current findings demonstrate cue-specific allocentric positional coding in the human RSC in the same navigation task for the first time and that spatial representations in the brain are contingent on specific experimental conditions.

How is GPS used? Understanding navigation system use and its relation to spatial ability.

Given how commonly GPS is now used in everyday navigation, it is surprising how little research has been dedicated to investigating variations in its use and how such variations may relate to navigation ability. The present study investigated general GPS dependence, how people report using GPS in various navigational scenarios, and the relationship between these measures and spatial abilities (assessed by self-report measures and the ability to learn the layout of a novel environment). GPS dependence is an individual's perceived need to use GPS in navigation, and GPS usage is the frequency with which they report using different functions of GPS. The study also assessed whether people modulate reported use of GPS as a function of their familiarity with the location in which they are navigating. In 249 participants over two preregistered studies, reported GPS dependence was negatively correlated with objective navigation performance and self-reported sense of direction, and positively correlated with spatial anxiety. Greater reported use of GPS for turn-by-turn directions was associated with a poorer sense of direction and higher spatial anxiety. People reported using GPS most frequently for time and traffic estimation, regardless of ability. Finally, people reported using GPS less, regardless of ability, when they were more familiar with an environment. Collectively these findings suggest that people moderate their use of GPS, depending on their knowledge, ability, and confidence in their own abilities, and often report using GPS to augment rather than replace spatial environmental knowledge.

Maze runners: monkeys show restricted Arabic numeral summation during computerized two-arm maze performance.

Mazes have been used in many forms to provide compelling results showcasing nonhuman animals' capacities for spatial navigation, planning, and numerical competence. The current study presented computerized two-arm mazes to four rhesus macaques. Using these mazes, we assessed whether the monkeys could maximize rewards by overcoming mild delays in gratification and sum the values of Arabic numerals. Across four test phases, monkeys used a joystick controller to choose one of two maze arms on the screen. Each maze arm contained zero, one or two Arabic numerals, and any numerals in the chosen maze arm provided the monkeys with rewards equivalent to the value of those numerals. When deciding which arm to enter, monkeys had to consider distance to numerals and numeral value. In some tests, gaining the maximum reward required summing the value of two numerals within a given arm. All four monkeys successfully maximized reward when comparing single numerals and when comparing arms that each contained two numerals. However, some biases occurred that were suboptimal: the largest single numeral and the delay of reward (by placing numerals farther into an arm from the start location) sometimes interfered with the monkeys' abilities to optimize. These results indicate that monkeys experience difficulties with inhibition toward single, high valence stimuli in tasks where those stimuli must be considered in relation to overall value when represented by symbolic stimuli such as numerals.

Individual differences in emerging adults' spatial abilities: What role do affective factors play?

Spatial ability is defined as a cognitive or intellectual skill used to represent, transform, generate, and recall information of an object or the environment. Individual differences across spatial tasks have been strongly linked to science, technology, engineering, and mathematics (STEM) interest and success. Several variables have been proposed to explain individual differences in spatial ability, including affective factors such as one's confidence and anxiety. However, research is lacking on whether affective variables such as confidence and anxiety relate to individual differences in both a mental rotation task (MRT) and a perspective-taking and spatial orientation task (PTSOT). Using a sample of 100 college students completing introductory STEM courses, the present study investigated the effects of self-reported spatial confidence, spatial anxiety, and general anxiety on MRT and PTSOT. Spatial confidence, after controlling for effects of general anxiety and biological sex, was significantly related to performance on both the MRT and PTSOT. Spatial anxiety, after controlling for effects of general anxiety and biological sex, was not related to either PTSOT or MRT scores. Together these findings suggest some affective factors, but not others, contribute to spatial ability performance to a degree that merits advanced investigation in future studies.

Parahippocampal neurons encode task-relevant information for goal-directed navigation.

A behavioral strategy crucial to survival is directed navigation to a goal, such as a food or home location. One potential neural substrate for supporting goal-directed navigation is the parahippocampus, which contains neurons that represent an animal's position, orientation, and movement through the world, and that change their firing activity to encode behaviorally relevant variables such as reward. However, little prior work on the parahippocampus has considered how neurons encode variables during goal-directed navigation in environments that dynamically change. Here, we recorded single units from rat parahippocampal cortex while subjects performed a goal-directed task. The maze dynamically changed goal-locations via a visual cue on a trial-to-trial basis, requiring subjects to use cue-location associations to receive reward. We observed a mismatch-like signal, with elevated neural activity on incorrect trials, leading to rate-remapping. The strength of this remapping correlated with task performance. Recordings during open-field foraging allowed us to functionally define navigational coding for a subset of the neurons recorded in the maze. This approach revealed that head-direction coding units remapped more than other functional-defined units. Taken together, this work thus raises the possibility that during goal-directed navigation, parahippocampal neurons encode error information reflective of an animal's behavioral performance.

Transforming a head direction signal into a goal-oriented steering command.

To navigate, we must continuously estimate the direction we are headed in, and we must correct deviations from our goal1. Direction estimation is accomplished by ring attractor networks in the head direction system2,3. However, we do not fully understand how the sense of direction is used to guide action. Drosophila connectome analyses4,5 reveal three cell populations (PFL3R, PFL3L and PFL2) that connect the head direction system to the locomotor system. Here we use imaging, electrophysiology and chemogenetic stimulation during navigation to show how these populations function. Each population receives a shifted copy of the head direction vector, such that their three reference frames are shifted approximately 120° relative to each other. Each cell type then compares its own head direction vector with a common goal vector; specifically, it evaluates the congruence of these vectors via a nonlinear transformation. The output of all three cell populations is then combined to generate locomotor commands. PFL3R cells are recruited when the fly is oriented to the left of its goal, and their activity drives rightward turning; the reverse is true for PFL3L. Meanwhile, PFL2 cells increase steering speed, and are recruited when the fly is oriented far from its goal. PFL2 cells adaptively increase the strength of steering as directional error increases, effectively managing the tradeoff between speed and accuracy. Together, our results show how a map of space in the brain can be combined with an internal goal to generate action commands, via a transformation from world-centric coordinates to body-centric coordinates.

Effects of estrogen on spatial navigation and memory.

RATIONALE: Animal studies suggest that the so-called "female" hormone estrogen enhances spatial navigation and memory. This contradicts the observation that males generally out-perform females in spatial navigation and tasks involving spatial memory. A closer look at the vast number of studies actually reveals that performance differences are not so clear. OBJECTIVES: To help clarify the unclear performance differences between men and women and the role of estrogen, we attempted to isolate organizational from activational effects of estrogen on spatial navigation and memory. METHODS: In a double-blind, placebo-controlled study, we tested the effects of orally administered estradiol valerate (E2V) in healthy, young women in their low-hormone menstrual cycle phase, compared to healthy, young men. Participants performed several first-person, environmentally rich, 3-D computer games inspired by spatial navigation and memory paradigms in animal research. RESULTS: We found navigation behavior suggesting that sex effects dominated any E2 effects with men performing better with allocentric strategies and women with egocentric strategies. Increased E2 levels did not lead to general improvements in spatial ability in either sex but to behavioral changes reflecting navigation flexibility. CONCLUSION: Estrogen-driven differences in spatial cognition might be better characterized on a spectrum of navigation flexibility rather than by categorical performance measures or skills.

Assessing Human Spatial Navigation in a Virtual Space and its Sensitivity to Exercise.

Spatial navigation (SN) is the ability to locomote through the environment, which requires an understanding of where one is located in time and space. This capacity is known to rely on the sequential firing of place cells within the hippocampus. SN is an important behavior to investigate as this process deteriorates with age, especially in neurodegenerative disorders. However, the investigation of SN is limited by the lack of sophisticated behavioral techniques to assess this hippocampal-dependent task. Therefore, the goal of this protocol was to develop a novel, real-world approach to studying SN in humans. Specifically, an active virtual SN task was developed using a cross-platform game engine. During the encoding phase, participants navigated their way through a virtual city to locate landmarks. During the remembering phase, participants remembered where these reward locations were and delivered items to these locations. Time to find each location was captured and episodic memory was assessed by a free recall phase, including aspects of place, order, item, and association. Movement behavior (x, y, and z coordinates) was assessed through an asset available in the game engine. Importantly, results from this task demonstrate that it accurately captures both spatial learning and memory abilities as well as episodic memory. Further, findings indicate that this task is sensitive to exercise, which improves hippocampal functioning. Overall, the findings suggest a novel way to track human hippocampal functioning over the course of time, with this behavior being sensitive to physical activity training paradigms.

Converting an allocentric goal into an egocentric steering signal.

Neuronal signals that are relevant for spatial navigation have been described in many species1-10. However, a circuit-level understanding of how such signals interact to guide navigational behaviour is lacking. Here we characterize a neuronal circuit in the Drosophila central complex that compares internally generated estimates of the heading and goal angles of the fly-both of which are encoded in world-centred (allocentric) coordinates-to generate a body-centred (egocentric) steering signal. Past work has suggested that the activity of EPG neurons represents the fly's moment-to-moment angular orientation, or heading angle, during navigation2,11. An animal's moment-to-moment heading angle, however, is not always aligned with its goal angle-that is, the allocentric direction in which it wishes to progress forward. We describe FC2 cells12, a second set of neurons in the Drosophila brain with activity that correlates with the fly's goal angle. Focal optogenetic activation of FC2 neurons induces flies to orient along experimenter-defined directions as they walk forward. EPG and FC2 neurons connect monosynaptically to a third neuronal class, PFL3 cells12,13. We found that individual PFL3 cells show conjunctive, spike-rate tuning to both the heading angle and the goal angle during goal-directed navigation. Informed by the anatomy and physiology of these three cell classes, we develop a model that explains how this circuit compares allocentric heading and goal angles to build an egocentric steering signal in the PFL3 output terminals. Quantitative analyses and optogenetic manipulations of PFL3 activity support the model. Finally, using a new navigational memory task, we show that flies expressing disruptors of synaptic transmission in subsets of PFL3 cells have a reduced ability to orient along arbitrary goal directions, with an effect size in quantitative accordance with the prediction of our model. The biological circuit described here reveals how two population-level allocentric signals are compared in the brain to produce an egocentric output signal that is appropriate for motor control.

[Spatial navigation method based on the entorhinal-hippocampal-prefrontal information transmission circuit of rat's brain].

Physiological studies have revealed that rats perform spatial localization relying on grid cells and place cells in the entorhinal-hippocampal CA3 structure. The dynamic connection between the entorhinal-hippocampal structure and the prefrontal cortex is crucial for navigation. Based on these findings, this paper proposes a spatial navigation method based on the entorhinal-hippocampal-prefrontal information transmission circuit of the rat's brain, with the aim of endowing the mobile robot with strong spatial navigation capability. Using the hippocampal CA3-prefrontal spatial navigation model as a foundation, this paper constructed a dynamic self-organizing model with the hippocampal CA1 place cells as the basic unit to optimize the navigation path. The path information was then fed back to the impulse neural network via hippocampal CA3 place cells and prefrontal cortex action neurons, improving the convergence speed of the model and helping to establish long-term memory of navigation habits. To verify the validity of the method, two-dimensional simulation experiments and three-dimensional simulation robot experiments were designed in this paper. The experimental results showed that the method presented in this paper not only surpassed other algorithms in terms of navigation efficiency and convergence speed, but also exhibited good adaptability to dynamic navigation tasks. Furthermore, our method can be effectively applied to mobile robots.

A meta-analytic review of the relation between spatial anxiety and spatial skills.

Spatial skills are key predictors of achievement in science, technology, engineering, and mathematics disciplines, despite being acquired through everyday life and not formally taught in schools. Spatial skills include a diverse group of abilities broadly related to reasoning about properties of space such as distance and direction. Recently, more research has investigated the link between spatial skills and spatial anxiety, defined as a fear or apprehension felt when engaged in spatial thinking. There has yet to be a meta-analytic review summarizing these findings. Thus, the goal of this preregistered meta-analytic review is to provide an estimate of the size of the relation between spatial anxiety and spatial skills while considering several moderators (grade/age group, sex, spatial skills measure/subtype, spatial anxiety measure/subtype, geographical region of sample, publication type/year, and risk of bias). Analyzing 283 effect sizes accumulated from research conducted between 1994 and 2020, we found a small, negative, and statistically significant (r = -.14) correlation between spatial anxiety and spatial skills. Results showed that effect sizes including mental manipulation anxiety, scalar comparison anxiety, and navigation skill were often significantly stronger than effect sizes including measures of other subtypes. The magnitude of the relation was not significantly different in children and adults, though effect sizes tended to be weaker for younger samples (r = -.08). Our results are consistent with previous findings of a significant relation between spatial anxiety and skills, and this work bridges a gap in the existing research, lending support to future research efforts investigating spatial cognition. (PsycInfo Database Record (c) 2024 APA, all rights reserved).