The relationship between object-based spatial ability and virtual navigation performance.

Spatial navigation is a multi-faceted behaviour drawing on many different aspects of cognition. Visuospatial abilities, such as mental rotation and visuospatial working memory, in particular, may be key factors. A range of tests have been developed to assess visuospatial processing and memory, but how such tests relate to navigation ability remains unclear. This understanding is important to advance tests of navigation for disease monitoring in various disorders (e.g., Alzheimer's disease) where spatial impairment is an early symptom. Here, we report the use of an established mobile gaming app, Sea Hero Quest (SHQ), as a measure of navigation ability in a sample of young, predominantly female university students (N = 78; 20; female = 74.3%; mean age = 20.33 years). We used three separate tests of navigation embedded in SHQ: wayfinding, path integration and spatial memory in a radial arm maze. In the same participants, we also collected measures of mental rotation (Mental Rotation Test), visuospatial processing (Design Organization Test) and visuospatial working memory (Digital Corsi). We found few strong correlations across our measures. Being good at wayfinding in a virtual navigation test does not mean an individual will also be good at path integration, have a superior memory in a radial arm maze, or rate themself as having a strong sense of direction. However, we observed that participants who were good in the wayfinding task of SHQ tended to perform well on the three visuospatial tasks examined here, and to also use a landmark strategy in the radial maze task. These findings help clarify the associations between different abilities involved in spatial navigation.

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.

Associations Between Video Game Engagement and ADHD Symptoms in Early Adolescence.

OBJECTIVE: We aim to investigate the direction of causality of the association between adolescent video game playing and later development of ADHD symptoms using a population-based sample of Canadian Youth. METHOD: The present study is based on longitudinal cohort data (N = 1,467). Youth self-reported weekly hours of video game playing as well as ADHD symptoms at both 12 and 13 years of age. RESULTS: Cross-lagged panel model were estimated to examine how adolescent video game playing prospectively contributes to ADHD symptoms while simultaneously considering how adolescent ADHD symptoms may prospectively contribute to videogame playing. Analyses revealed a significant positive association between adolescent video games playing at age 12 and ADHD symptoms at age 13. Youth ADHD symptoms at age 12 did not predict video game use at age 13. CONCLUSION: Our results help clarify the direction of causality of the association between video game playing and ADHD symptoms and provide evidence that video game playing can represent a risk factor for the development of attention problems in early adolescence.

The BDNF val66met polymorphism is associated with decreased use of landmarks and decreased fMRI activity in the hippocampus during virtual navigation.

People can navigate in a new environment using multiple strategies dependent on different memory systems. A series of studies have dissociated between hippocampus-dependent 'spatial' navigation and habit-based 'response' learning mediated by the caudate nucleus. The val66met polymorphism of the brain-derived neurotrophic factor (BDNF) gene leads to decreased secretion of BDNF in the brain, including the hippocampus. Here, we aim to investigate the role of the BDNF val66met polymorphism on virtual navigation behaviour and brain activity in healthy older adults. A total of 139 healthy older adult participants (mean age = 65.8 ± 4.4 years) were tested in this study. Blood samples were collected, and BDNF val66met genotyping was performed. Participants were divided into two genotype groups: val homozygotes and met carriers. Participants were tested on virtual dual-solution navigation tasks in which they could use either a hippocampus-dependent spatial strategy or a caudate nucleus-dependent response strategy to solve the task. A subset of the participants (n = 66) were then scanned in a 3T functional magnetic resonance imaging (fMRI) scanner while engaging in another dual-solution navigation task. BDNF val/val individuals and met carriers did not differ in learning performance. However, the two BDNF groups differed in learning strategy. BDNF val/val individuals relied more on landmarks to remember target locations (i.e., increased use of flexible spatial learning), while met carriers relied more on sequences and patterns to remember target locations (i.e., increased use of inflexible response learning). Additionally, BDNF val/val individuals had more fMRI activity in the hippocampus compared with BDNF met carriers during performance on the navigation task. This is the first study to show in older adults that BDNF met carriers use alternate learning strategies from val/val individuals and to identify differential brain activation of this behavioural difference between the two groups.

Differential stress response to psychological and physical stressors in children using spatial versus response-dependent navigation strategies.

Previous work from our lab has shown that basal cortisol levels are different between healthy young adults who spontaneously use caudate nucleus-dependent response strategies compared to young adults who use hippocampus-dependent spatial navigation strategies. Young adults who use caudate nucleus dependent strategies display lower basal cortisol levels compared to those who use hippocampus-dependent strategies. In the current study, we assessed navigation strategies in children using a virtual navigation task and measured cortisol at baseline as well as cortisol reactivity to both a psychological and to a physical stressor. Replicating what is observed in adults, we found that children who used caudate nucleus-dependent navigation strategies displayed lower cortisol levels at baseline compared to those who used hippocampus-dependent strategies. The psychological stressor, knowledge that a blood draw would be performed by a nurse, caused a significant increase in cortisol uniquely in response learners. The physical stressor, the actual blood draw, produced a significant increase in cortisol amongst spatial learners that was then comparable to levels observed in response learners. Lower baseline cortisol and higher cortisol psychological stress response observed amongst children who used response strategies may therefore reflect early biological changes during development which may have an impact later in life when considering risk for neuropsychiatric disorders.

Negative correlation between grey matter in the hippocampus and caudate nucleus in healthy aging.

Neurobiological changes that occur with aging include a reduction in function and volume of the hippocampus. These changes were associated with corresponding memory deficits in navigation tasks. However, navigation can involve different strategies that are dependent on the hippocampus and caudate nucleus. The proportion of people using hippocampus-dependent spatial strategies decreases across the lifespan. As such, the decrease in spatial strategies, and corresponding increase in caudate nucleus-dependent response strategies with age, may play a role in the observed neurobiological changes in the hippocampus. Furthermore, we previously showed a negative correlation between grey matter in the hippocampus and caudate nucleus/striatum in mice, young adults, and in individuals diagnosed with Alzheimer's disease. As such, we hypothesized that this negative relationship between the two structures would be present during normal aging. The aim of the current study was to investigate this gap in the literature by studying the relationship between grey matter in the hippocampus and caudate nucleus of the striatum, in relation to each other and to navigation strategies, during healthy aging. Healthy older adults (N = 39) were tested on the Concurrent Spatial Discrimination Learning Task (CSDLT), a virtual radial task that dissociates between spatial and response strategies. A regression of strategies against structural MRIs showed for the first time in older adults that the response strategy was associated with higher amounts of grey matter in the caudate nucleus. As expected, the spatial strategy correlated with grey matter in the hippocampus, which was negatively correlated with grey matter in the caudate nucleus. Interestingly, a sex difference emerged showing that among older adult response learners, women have the least amount of grey matter in the hippocampus, which is a known risk for Alzheimer's disease. This difference was absent among spatial learners. These results are discussed in the context of the putative protective role of spatial memory against grey matter loss in the hippocampus, especially in women.

Habitual use of GPS negatively impacts spatial memory during self-guided navigation.

Global Positioning System (GPS) navigation devices and applications have become ubiquitous over the last decade. However, it is unclear whether using GPS affects our own internal navigation system, or spatial memory, which critically relies on the hippocampus. We assessed the lifetime GPS experience of 50 regular drivers as well as various facets of spatial memory, including spatial memory strategy use, cognitive mapping, and landmark encoding using virtual navigation tasks. We first present cross-sectional results that show that people with greater lifetime GPS experience have worse spatial memory during self-guided navigation, i.e. when they are required to navigate without GPS. In a follow-up session, 13 participants were retested three years after initial testing. Although the longitudinal sample was small, we observed an important effect of GPS use over time, whereby greater GPS use since initial testing was associated with a steeper decline in hippocampal-dependent spatial memory. Importantly, we found that those who used GPS more did not do so because they felt they had a poor sense of direction, suggesting that extensive GPS use led to a decline in spatial memory rather than the other way around. These findings are significant in the context of society's increasing reliance on GPS.

Opposing effects of cortisol on learning and memory in children using spatial versus response-dependent navigation strategies.

Previous studies showed that healthy young adults who spontaneously use caudate nucleus-dependent strategies on a virtual navigation task, have significantly lower basal levels of cortisol compared with adults who use hippocampus-dependent spatial navigation strategies. In the current paper, we assessed the relation between basal cortisol levels and learning using a virtual navigation task in children. We show that basal cortisol level has a differential effect on learning and memory between children using spatial and response navigation strategies. Specifically, cortisol was found to be beneficial for learning performance in children using spatial strategies, such that higher levels of cortisol were associated with more efficient learning in a virtual maze. In contrast, cortisol had a deleterious effect on learning the virtual maze in children using response strategies, such that higher cortisol levels were associated with increased spatial working memory errors. Based on these results, individual differences in navigation strategy could help explain contradictory results in the literature showing that cortisol can have either a positive or negative association with learning and memory performance.

Theta rhythm across the species: Bridging inconsistencies with a multiple memory systems approach.

The discovery of movement-modulated 7-8 Hz theta rhythm in rodents provided one of the earliest indications of synchronicity of neuronal firing in the hippocampus. Subsequent research expanded on this finding on theta rhythm and its role in other domains such as spatial navigation and memory. Nevertheless, discrepancies among animal models posed the question of how well the animal literature represents human mechanisms. Technological advances have since facilitated research taking place directly in humans, typically neurosurgical patients implanted with intracranial electrodes. Human studies have observed lower frequency oscillations in participants engaged in virtual spatial navigation studies, compared to the 7-8 Hz oscillations seen in rodents. Recently, research in humans engaged in real-world task demonstrating 7-9 Hz oscillations infer that the previously observed lower frequency theta may have been constrained by the absence of movement-related processing that occurs in physical activities. Together, these findings suggest that humans may indeed be more similar to rodent models than previously reported when completing tasks more analogous to those used in rodent experiments. This review summarizes early work on theta rhythm across species and outlines certain remaining discrepancies as well as a novel proposed hypothesis of the behavioral correlates of theta rhythm, taking a multiple memory systems perspective. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Spontaneous spatial navigation circuitry in schizophrenia spectrum disorders.

Spatial memory is core to wayfinding and everyday memory. Interestingly, individuals with schizophrenia using spatial navigation strategies (cognitive mapping) are impaired, whereas those using response-based (e.g., single-landmark) strategies show relatively intact memory performance. We observed abnormal brain communication in schizophrenia participants who used a spatial strategy during a virtual-reality navigation task, particularly between temporal and frontal brain regions. In contrast, schizophrenia participants using a response strategy recruited similar brain systems to healthy participants, but to a greater extent to support memory performance. These findings highlight that strategy use is an important consideration for understanding memory systems and navigation in schizophrenia.

Caudate nucleus-dependent navigation strategies are associated with increased risk-taking and set-shifting behavior.

When people navigate, they use strategies dependent on one of two memory systems. The hippocampus-based spatial strategy consists of using multiple landmarks to create a cognitive map of the environment. In contrast, the caudate nucleus-based response strategy is based on the memorization of a series of turns. Importantly, response learners display more gray matter and functional activity in the caudate nucleus and less gray matter in the hippocampus. In parallel, the caudate nucleus is involved in decision-making by mediating attention toward rewards and in set-shifting by mediating preparatory actions. The present study, therefore, examined the link between navigational strategy use, that are associated with gray matter differences in the caudate nucleus and hippocampus, and decision-making and set-shifting performance. Fifty-three participants completed the 4 on 8 virtual maze, the Iowa Gambling Task (IGT), the Wisconsin Card Sorting Test-64 (WCST-64), and a task-switching test. The results revealed that people who use response strategies displayed increased risk-taking behavior in the IGT compared to the people using hippocampus-dependent spatial strategies. Response strategy was also associated with enhanced set-shifting performance in the WCST-64 and task-switching test. These results confirm that risk-taking and set-shifting behavior, that are differentially impacted by the caudate nucleus and hippocampus memory systems, can be predicted by navigational strategy.

Autistic traits in neurotypical individuals are associated with increased landmark use during navigation.

People adopt two distinct learning strategies during navigation. "Spatial learners" navigate by building a cognitive map using environmental landmarks, and display more grey matter in the hippocampus. Conversely, "response learners" memorize a series of rigid turns to navigate and display more grey matter in the caudate nucleus of the striatum. Evidence has linked these two structures with autism spectrum disorder (ASD) and autistic traits in non-clinical populations. Both people with ASD and neurotypical people with higher levels of autistic traits have been shown to display more grey matter in the hippocampus and less functional activity in the caudate nucleus. We therefore tested 56 healthy participants who completed the Autism Quotient (AQ) Scale and the 4-on-8 Virtual Maze (4/8 VM), which determines the reliance on landmarks during navigation. We found that people who relied on landmarks during navigation also displayed significantly higher scores on the AQ Scale. Because spatial strategies are associated with increased attention to environmental landmark use and are supported by the hippocampus, our results provide a potential behavioral mechanism linking higher autistic traits (e.g., increased attention to detail and increased sensory processes) to increased hippocampal grey matter.

Fimbria-Fornix Volume Is Associated With Spatial Memory and Olfactory Identification in Humans.

White matter pathways that surround the hippocampus comprise its afferent and efferent connections, and are therefore crucial in mediating the function of the hippocampus. We recently demonstrated a role for the hippocampus in both spatial memory and olfactory identification in humans. In the current study, we focused our attention on the fimbria-fornix white matter bundle and investigated its relationship with spatial memory and olfactory identification. We administered a virtual navigation task and an olfactory identification task to 55 young healthy adults and measured the volume of the fimbria-fornix. We found that the volume of the right fimbria-fornix and its subdivisions is correlated with both navigational learning and olfactory identification in those who use hippocampus-based spatial memory strategies, and not in those who use caudate nucleus-based navigation strategies. These results are consistent with our recent finding that spatial memory and olfaction rely on similar neural networks and structures.

An intrinsic association between olfactory identification and spatial memory in humans.

It was recently proposed that olfaction evolved to aid navigation. Consistent with this hypothesis, olfactory identification and spatial memory are linked to overlapping brain areas which include the orbitofrontal cortex and hippocampus. However, the relationship between these two processes has never been specifically investigated. Here, we show that olfactory identification covaries with spatial memory in humans. We also found that the cortical thickness of the left medial orbitofrontal cortex, and the volume of the right hippocampus, predict both olfactory identification and spatial memory. Finally, we demonstrate deficits in both olfactory identification and spatial memory in patients with lesions of the medial orbitofrontal cortex. Our findings reveal an intrinsic relationship between olfaction and spatial memory that is supported by a shared reliance on the hippocampus and medial orbitofrontal cortex. This relationship may find its roots in the parallel evolution of the olfactory and hippocampal systems.

Global Determinants of Navigation Ability.

Human spatial ability is modulated by a number of factors, including age [1-3] and gender [4, 5]. Although a few studies showed that culture influences cognitive strategies [6-13], the interaction between these factors has never been globally assessed as this requires testing millions of people of all ages across many different countries in the world. Since countries vary in their geographical and cultural properties, we predicted that these variations give rise to an organized spatial distribution of cognition at a planetary-wide scale. To test this hypothesis, we developed a mobile-app-based cognitive task, measuring non-verbal spatial navigation ability in more than 2.5 million people and sampling populations in every nation state. We focused on spatial navigation due to its universal requirement across cultures. Using a clustering approach, we find that navigation ability is clustered into five distinct, yet geographically related, groups of countries. Specifically, the economic wealth of a nation was predictive of the average navigation ability of its inhabitants, and gender inequality was predictive of the size of performance difference between males and females. Thus, cognitive abilities, at least for spatial navigation, are clustered according to economic wealth and gender inequalities globally, which has significant implications for cross-cultural studies and multi-center clinical trials using cognitive testing.

Habitual action video game players display increased cortical thickness in the dorsal anterior cingulate cortex.

Action video game players (aVGPs) display increased performance in attention-based tasks and enhanced procedural motor learning. In parallel, the anterior cingulate cortex (ACC) is centrally implicated in specific types of reward-based learning and attentional control, the execution or inhibition of motor commands, and error detection. These processes are hypothesized to support aVGP in-game performance and enhanced learning though in-game feedback. We, therefore, tested the hypothesis that habitual aVGPs would display increased cortical thickness compared with nonvideo game players (nonVGPs). Results showed that the aVGP group (n=17) displayed significantly higher levels of cortical thickness specifically in the dorsal ACC compared with the nonVGP group (n=16). Results are discussed in the context of previous findings examining video game experience, attention/performance, and responses to affective components such as pain and fear.

Healthy versus Entorhinal Cortical Atrophy Identification in Asymptomatic APOE4 Carriers at Risk for Alzheimer's Disease.

Early detection of Alzheimer's disease (AD) has been challenging as current biomarkers are invasive and costly. Strong predictors of future AD diagnosis include lower volume of the hippocampus and entorhinal cortex, as well as the ɛ4 allele of the Apolipoprotein E gene (APOE) gene. Therefore, studying functions that are critically mediated by the hippocampus and entorhinal cortex, such as spatial memory, in APOE ɛ4 allele carriers, may be key to the identification of individuals at risk of AD, prior to the manifestation of cognitive impairments. Using a virtual navigation task developed in-house, specifically designed to assess spatial versus non-spatial strategies, the current study is the first to differentiate functional and structural differences within APOE ɛ4 allele carriers. APOE ɛ4 allele carriers that predominantly use non-spatial strategies have decreased fMRI activity in the hippocampus and increased atrophy in the hippocampus, entorhinal cortex, and fimbria compared to APOE ɛ4 allele carriers who use spatial strategies. In contrast, APOE ɛ4 allele carriers who use spatial strategies have grey matter levels comparable to non-APOE ɛ4 allele carriers. Furthermore, in a leave-one-out analysis, grey matter in the entorhinal cortex could predict navigational strategy with 92% accuracy.

Playing Super Mario 64 increases hippocampal grey matter in older adults.

Maintaining grey matter within the hippocampus is important for healthy cognition. Playing 3D-platform video games has previously been shown to promote grey matter in the hippocampus in younger adults. In the current study, we tested the impact of 3D-platform video game training (i.e., Super Mario 64) on grey matter in the hippocampus, cerebellum, and the dorsolateral prefrontal cortex (DLPFC) of older adults. Older adults who were 55 to 75 years of age were randomized into three groups. The video game experimental group (VID; n = 8) engaged in a 3D-platform video game training over a period of 6 months. Additionally, an active control group took a series of self-directed, computerized music (piano) lessons (MUS; n = 12), while a no-contact control group did not engage in any intervention (CON; n = 13). After training, a within-subject increase in grey matter within the hippocampus was significant only in the VID training group, replicating results observed in younger adults. Active control MUS training did, however, lead to a within-subject increase in the DLPFC, while both the VID and MUS training produced growth in the cerebellum. In contrast, the CON group displayed significant grey matter loss in the hippocampus, cerebellum and the DLPFC.

Hippocampus-dependent spatial learning is associated with higher global cognition among healthy older adults.

Cognitive deficits in normal aging have been associated with atrophy of the hippocampus. As such, methods to detect early dysfunction of the hippocampus have become valuable, if not indispensable, to early intervention. The hippocampus is critical for spatial memory and is among the first structures to atrophy with aging. Despite the presence of navigation deficits in aging, few studies have looked at the association between wayfinding ability, navigation strategies, general cognitive function, and hippocampal volume. In the current study we investigated whether better general cognitive function is associated with the use of hippocampal-dependent spatial strategies, better spatial memory, and increased hippocampal volume. We also investigated, within older adults, the effects of aging on spatial memory. Healthy older adults (N = 107) were tested on a virtual wayfinding task and a dual-solution navigation task that can be solved using either a hippocampal-dependent spatial strategy or a caudate nucleus-dependent response strategy. Participants were also administered the Montreal Cognitive Assessment (MoCA), a test that measures general cognition and is sensitive to dementia. A structural MRI was administered to a sub-set of participants (n = 49) and hippocampal volume was calculated using a Multiple Automatically Generated Templates (MAGeT) Brain algorithm. We found that age was negatively associated with wayfinding ability and hippocampal volume. On the wayfinding task, participants with higher MoCA scores found more target locations and travelled shorter distances. We also found a significant association between higher MoCA scores and spatial strategy use. MoCA scores, spatial memory ability, and spatial strategy use all positively correlated with a larger hippocampal volume. These results confirm that with age there is a decrease in spatial memory, which is consistent with decreased volume in the hippocampus with aging. Furthermore, better general cognitive function is associated with better wayfinding ability and increased use of hippocampal-dependent spatial strategies.

Hippocampal activation and memory performance in schizophrenia depend on strategy use in a virtual maze.

Different strategies may be spontaneously adopted to solve most navigation tasks. These strategies are associated with dissociable brain systems. Here, we use brain-imaging and cognitive tasks to test the hypothesis that individuals living with Schizophrenia Spectrum Disorders (SSD) have selective impairment using a hippocampal-dependent spatial navigation strategy. Brain activation and memory performance were examined using functional magnetic resonance imaging (fMRI) during the 4-on-8 virtual maze (4/8VM) task, a human analog of the rodent radial-arm maze that is amenable to both response-based (egocentric or landmark-based) and spatial (allocentric, cognitive mapping) strategies to remember and navigate to target objects. SSD (schizophrenia and schizoaffective disorder) participants who adopted a spatial strategy performed more poorly on the 4/8VM task and had less hippocampal activation than healthy comparison participants using either strategy as well as SSD participants using a response strategy. This study highlights the importance of strategy use in relation to spatial cognitive functioning in SSD. Consistent with a selective-hippocampal dependent deficit in SSD, these results support the further development of protocols to train impaired hippocampal-dependent abilities or harness non-hippocampal dependent intact abilities.