Cognitive maps for a non-Euclidean environment: path integration and spatial memory on a sphere

Adequate homing is essential for the survival of any animal when it leaves its home to find prey or a mate. There are several strategies by which homing can be carried out: (a) retrace the outbound path; (b) use a 'cognitive map'; or (c) use path integration (PI). Here, I review the state of the art of research on spiders (Araneae) and whip spiders (Amblypygi) homing behaviour. The main strategy described in the literature as being used by these arachnids is PI. Behavioural and neural substrates of PI are described in a small group of spider families (Agelenidae, Lycosidae, Gnaphosidae, Ctenidae and Theraphosidae) and a whip spider family (Phrynidae). In spiders, the cues used to detect the position of the animal relative to its home are the position of the sun, polarized light patterns, web elasticity and landmarks. In whip spiders, the cues used are olfactory, tactile and, with a more minor role, visual. The use of a magnetic field in whip spiders has been rejected both with field and laboratory studies. Concerning the distance walked in PI, the possibility of using optic flow and idiothetic information in spiders is considered. The studies about outbound and inbound paths in whip spiders seem to suggest they do not follow the PI rules. As a conclusion, these arachnids' navigation relies on multimodal cues. We have detailed knowledge about the sensory origin (visual, olfactory, mechanosensory receptors) of neural information, but we are far from knowing the central neural structures where sensory information is integrated.

BackgroundThe entorhinal cortex (EC) contains spatially modulated cells, so called grid cells, and plays a central role in spatial navigation. Studies show that tauopathy in the EC is already observed in the early stages of Alzheimer's disease (AD) and is responsible for impairments in spatial memory performance. Moreover, recent studies demonstrate that young, healthy volunteers with the APOE‐ε4‐allele, a genetic risk factor for AD, show impaired grid‐like representations in the EC and reduced path integration performance in environments without spatial cues. People with subjective cognitive decline (SCD) perceive a subjective deterioration in their cognitive memory performance with unimpaired performance on standardized neuropsychological tests. SCD corresponds to the recently defined stage 2 of AD and is also a risk factor for dementia. Here, we tested whether subjects with SCD show path integration impairment, presumably related to malfunctioning in the EC.Method68 participants (31 SCD patients recruited through a memory clinic, age: 68.8 ± 9.2; 37 controls without SCD, age: 69.1 ± 7.9) performed a path integration task on a laptop. In addition, a neuropsychological test (CERAD+) was carried out to rule out an objective cognitive impairment.ResultThe two groups did not differ in age, sex, medical history and number of educational years. We replicated previous findings indicating better path integration performance with spatial cues such as boundaries and landmarks (F(2,128) = 20.83, P < 0.001). In addition, we showed that women performed worse than men (F(1,64) = 6.00, P = 0.017) and that path integration performance declined with increasing age (F(1,64) = 32.14, P < 0.001). There was no significant difference in performance between SCD and controls (F(1,64) = 2.20, P = 0.143).ConclusionGenerally, SCD was not associated with lower path integration performance. We are in the process of characterizing the sample based on plasma amyloid beta 42/40, NFL, pTau and APOE genotype to test, if AD biomarkers and genetic risk factors are associated with path integration performance.

This study used a dual task design to investigate the effects of two different types of cognitive tasks on stability (as measured by center of pressure displacement) in young vs older adults with and without a history of falls. Two secondary cognitive tasks, a sentence completion and a visual perceptual matching task, were used to produce changes in attention during quiet stance under flat vs compliant surface conditions in 20 healthy young adults, 20 healthy older adults, and 20 older adults with a history of imbalance and falls. Postural stability was quantified using forceplate measures of center of pressure (COP). Speed and accuracy of verbal response on the cognitive tasks were also quantified. During the simultaneous performance of a cognitive and postural task, decrements in performance were found in the postural stability measures rather than the cognitive measures for all three groups. While no differences were found between the young adults and the older healthy adults on the firm surface, no task condition, when task complexity was increased (either through the introduction of a secondary cognitive task, or a more challenging postural condition such as standing on the compliant surface), significant differences in postural stability between the two groups became apparent. In contrast to the young and healthy older adults, postural stability in older adults with a history of falls was significantly affected by both cognitive tasks. Results suggest that when postural stability is impaired, even relatively simple cognitive tasks can further impact balance. Results further suggest that the allocation of attention during the performance of concurrent tasks is complex; depending on many factors including the nature of both the cognitive and postural task, the goal of the subject and the instructions.

Over the past two decades, much research has been conducted to investigate whether humans are optimal when integrating sensory cues during spatial memory and navigational tasks. Although this work has consistently demonstrated optimal integration of visual cues (e.g., landmarks) with body-based cues (e.g., path integration) during human navigation, little work has investigated how cues of the same sensory type are integrated in spatial memory. A few recent studies have reported mixed results, with some showing very little benefit to having access to more than one landmark, and others showing that multiple landmarks can be optimally integrated in spatial memory. In the current study, we employed a combination of immersive and non-immersive virtual reality spatial memory tasks to test adult humans’ ability to integrate multiple landmark cues across six experiments. Our results showed that optimal integration of multiple landmark cues depends on the difficulty of the task, and that the presence of multiple landmarks can elicit an additional latent cue when estimating locations from a ground-level perspective, but not an aerial perspective.

Spatial memory is a fundamental cognitive function that enables humans and other species to encode and recall the locations of items in their environments. Humans employ diverse strategies to support spatial memory, including the use of cognitive maps. Cognitive maps are mental representations of the environment that organize its content along two or more continuous dimensions. In allocentric cognitive maps, these dimensions form a Cartesian coordinate system referenced to the environment. In egocentric cognitive maps, the dimensions form a polar coordinate system centered on the subject. To better understand how humans employ allocentric and egocentric cognitive maps for spatial memory, we performed a behavioral study with a novel task designed to directly and explicitly assess both types of cognitive maps. During encoding periods, participants navigated through a virtual environment and encountered objects at different locations. During recall periods, participants aimed at remembering these locations in abstract allocentric and egocentric coordinate systems. Our results show that relationships between the objects and the environment, such as their distance to boundaries and corners, were associated with allocentric memory performance. Relationships between the objects and the participant, including their distance and orientation to the participant's starting position, were linked to egocentric memory performance. Spatial feedback during recall supported performance within allocentric and egocentric domains, but not across domains. These findings are compatible with the notion that allocentric and egocentric cognitive maps operate as (partially) independent systems for spatial memory, each specialized in processing specific types of spatial relationships.

Path integration is a fundamental skill for navigation in both humans and animals. Despite recent advances in unraveling the neural basis of path integration in animal models, relatively little is known about how path integration operates at a neural level in humans. Previous attempts to characterize the neural mechanisms used by humans to visually path integrate have suggested a central role of the hippocampus in allowing accurate performance, broadly resembling results from animal data. However, in recent years both the central role of the hippocampus and the perspective that animals and humans share similar neural mechanisms for path integration has come into question. The present study uses a data driven analysis to investigate the neural systems engaged during visual path integration in humans, allowing for an unbiased estimate of neural activity across the entire brain. Our results suggest that humans employ common task control, attention and spatial working memory systems across a frontoparietal network during path integration. However, individuals differed in how these systems are configured into functional networks. High performing individuals were found to more broadly express spatial working memory systems in prefrontal cortex, while low performing individuals engaged an allocentric memory system based primarily in the medial occipito-temporal region. These findings suggest that visual path integration in humans over short distances can operate through a spatial working memory system engaging primarily the prefrontal cortex and that the differential configuration of memory systems recruited by task control networks may help explain individual biases in spatial learning strategies.

Neurodegenerative disease is common and frequently occurs in elderly patients. Previous studies have shown that ginsenoside Rg1 was able to inhibit senescent of brain, but the mechanism on the brain during the treatment remains elucidated. To study the mechanism of ginsenoside Rg1 in the process of anti-aging of brain, forty male SD rats were randomly divided into normal group, Rg1 normal group, brain aging model group and Rg1 brain aging model group, each group with 10 rats (brain aging model group: subcutaneous injection of D-galactose (120 mg kg(-1)), qd for 42 consecutive days; Rg1 brain aging model group: while copying the same test as that of brain aging model group, begin intraperitoneal injection of ginsenosides Rg1 (20 mg x kg(-1)) qd for 27 d from 16 d. Rg1 normal group: subcutaneous injection of the same amount of saline; begin intraperitoneal injection of ginsenosides Rg1 (20 mg x kg(-1)) qd for 27 d from 16 d. Normal: injected with an equal volume of saline within the same time. Perform the related experiment on the second day after finishing copying the model or the completion of the first two days of drug injections). Learning and memory abilities were measured by Morris water maze. The number of senescent cells was detected by SA-beta-Gal staining while the level of IL-1 and IL-6 proinflammatory cytokines in hippocampus were detected by ELISA. The activities of SOD, contents of GSH in hippo- campus were quantified by chromatometry. The change of telomerase activities and telomerase length were performed by TRAP-PCR and southern blotting assay, respectively. It is pointed that, in brain aging model group, the spatial learning and memory capacities were weaken, SA-beta-Gal positive granules increased in section of brain tissue, the activity of antioxidant enzyme SOD and the contents of GSH decreased in hippocampus, the level of IL-1 and IL-6 increased in hippocampus, while the length of telomere and the activity of telomerase decreased in hippocampus. Rats of Rg1 brain aging group had their spatial learning and memory capacities enhanced, SA-beta-Gal positive granules in section of brain tissue decreased, the activity of antioxidant enzyme SOD and the contents of GSH increased in hippocampus, the level of IL-1 and IL-6 in hippocampus decreased, the length contraction of telomere suppressed while the change of telomerase activity increased in hippocampus. Compared with that of normal group, the spatial learning and memory capacities were enhanced in Rg1 normal group, SA-beta-Gal positive granules in section of brain tissue decreased in Rg1 normal group, the level of IL-1 and IL-6 in hippocampus decreased in Rg1 normal group. The results indicated that improvement of antioxidant ability, regulating the level of proinflammatory cytokines and regulation of telomerase system may be the underlying anti-aging mechanism of Ginsenoside Rg1.

AimTo study the acute effect of a dietary multi-ingredient nootropic on cognitive performance in young healthy adults. We also analyzed the influence of the dietary multi-ingredient nootropic on emotional state, heart rate (HR), and heart rate variability (HRV).MethodsThis is a randomized, triple-blinded, placebo-controlled, crossover trial. In total, 26 young healthy adults (50% women; 24.9 ± 3.3 years old) ingested 10 g of a dietary multi-ingredient nootropic [Evo-Gamers®; Harrison Sport Nutrition (HSN), Granada, Spain] or placebo (maltodextrin) in a randomized order (clinicaltrials.gov No. NCT04790188). After 30 min of the ingestion, participants performed a battery of cognitive performance tests to measure the processing speed, inhibitory control, working memory, cognitive flexibility, creativity, and verbal fluency. The emotional status was assessed through questionnaires, and HR and HRV were measured using a heart rate monitor.ResultsIn comparison with placebo, the acute ingestion of the nootropic showed a significantly better response time in several cognitive tests (i.e., processing speed, inhibitory control, spatial working memory, and cognitive flexibility, all P < 0.05 and effect size range of 0.4–0.6). It also displayed a higher accuracy in the processing speed, the inhibitory control, and cognitive flexibility tests (all P < 0.05; effect size ranged from 0.4 to 0.6). Furthermore, the nootropic showed a higher creativity and positive emotions and lower sadness-depression emotions, whereas HR and HRV remained similar between placebo vs. nootropic conditions. However, there were no differences between the nootropic and placebo in verbal fluency, motivation, or anxiety (all P > 0.05).ConclusionAn acute ingestion of a dietary multi-ingredient nootropic enhances cognitive performance in comparison with placebo without negatively influencing HR or HRV in young healthy adults.

While much is known about the effects of dual tasking on cyclical and continuous motor performance (e.g., locomotion), there is a paucity of information on the effect of dual tasking on the initiation of movement. Therefore, the purpose of this study was to investigate the effect of a concurrent cognitive task on gait initiation in three groups: patients with Parkinson disease, healthy older adults, and healthy young adults. We examined the anticipatory postural adjustment displacements and velocities during single-task gait initiation as well as two dual-task conditions: (1) 0-back + gait initiation and (2) 2-back + gait initiation. The Parkinson disease group exhibited less anticipatory postural adjustment displacement and velocity than their aged-matched healthy peers and young adults during the single- and dual-task gait initiation settings (p < 0.05). Of interest was the finding of no additional effect on anticipatory postural adjustment displacement or velocity of gait initiation during the dual-task conditions in any group, including the Parkinson disease group. More traditionally studied gait/balance dual-task paradigms have demonstrated both motor and cognitive decline. Therefore, our results may suggest a prioritization of more "intentional" movement task (e.g., gait initiation) while dual tasking in Parkinson disease.

A Quarter of a Century of Place Cells

Effects of glucocorticoid and noradrenergic activity on spatial learning and spatial memory in healthy young adults

The Metabolic Cost of Walking (MCoW) is typically expressed either in terms of Gross Cost of Walking (GCoW) or Net Cost of Walking (NCoW). MCoW is defined as the metabolic energy expended per meter travelled and is an important variable in daily life. From the literature we can see that increased MCoW for elderly compared to young might lead to elderly becoming fatigued and sedentary. Increased fatigue and sedentarism limits their functional possibilities, thereby affecting the overall quality of life. The motivation for this doctoral project was that we wanted to know the reasons why elderly have a higher MCoW compared to young, especially during overground walking. We were interested in overground walking since it is the ecologically relevant mode of walking. However, before trying to know why elderly have a higher MCoW than young we wanted to see whether this finding of elevated MCoW for elderly was valid in the first place and if so, specifically for overground walking. To answer our research questions, we conducted three studies in this thesis. We started with a systematic review and meta-analysis and reported on this study in Chapter 1 of this thesis. Then we followed it up with two experimental studies and then reported on them in Chapters 2 and 3 of this thesis. To summarise, from the studies conducted in this thesis, we were able to show that the commonly reported elevation in MCoW for Older Adults (OA) over Young Adults (YA) is not due to age per se but is probably due to the differential reaction to treadmills by healthy YA and OA. In Chapters 2 and 3 we have shown that OA react differently to overground and treadmill walking (elevated MCoW on treadmills compared to overground) at their overground Preferred Walking Speed (PWS), which we directly imposed on the treadmills. YA do not react differently to overground and treadmill walking at the same speed as they have similar MCoW. Due to this differential reaction to overground and treadmill walking by YA and OA walking energetics are different between the two groups. In conclusion, through this thesis we have shown how to have age as the only differentiating factor between YA and OA while trying to learn about the differences in MCoW between the cohorts. There were no differences in anthropometrics, physical activity and fitness levels and overground PWS between our YA and OA. Our main finding is that we have shown there are no differences in overground MCoW between them. As overground walking is the ecologically relevant mode of walking, overground MCoW should be considered important. Due to the differential reaction of YA and OA to treadmills, treadmills are not suitable for comparison of MCoW between the two populations. The results of similar overground MCoW of YA and OA could have some clinical implications. For example, these results could be interpreted in the way that if people adopt a healthy and active lifestyle from an early age, when they grow old, they can have similar levels of PWS and MCoW like a young person. Comparable levels of PWS would generally mean that mobility and daily life gait will not be affected and similar levels of MCoW will mean that elderly will expend the same amount of energy after walking the same distance as a young person. Overall this will imply that elderly will be able to lead a normal healthy lifestyle, not become fatigued and sedentary, and we can achieve the goals of healthy aging in our society.

BackgroundThis study aimed to determine the effects of long-term running exercise on spatial learning, spatial memory, and cortical capillaries in aged rats.Material/MethodsFourteen-month-old female and male Sprague-Dawley rats were randomly divided into an exercised group (EG) and a non-exercised group (NG). The EG rats were trained on treadmill running for 4 or 14 months. The NG rats were housed under identical conditions without running. Spatial learning and memory were assessed with the Morris water maze. The cortical capillary parameters were quantitatively investigated using immunohistochemical and stereological methods.ResultsThe escaped latencies of the EG were significantly different from those of the NG in 18-month-old females and 28-month-old males (p<0.05). However, 28-month-old females and 18-month-old males showed no differences in escape latency between the EG and NG (p>0.05). In 28-month-old female rats, stereological techniques showed significant differences between the EG and NG in the cortical capillary volume (median, 22.55 vs. 11.42, p<0.05) and the cortical capillary surface area (median, 7474.13 vs. 3935.90, p<0.05). In 28-month-old male rats, the EG had a significantly longer total cortical capillary length (median, 530.35 vs. 156.27, p<0.05), significantly larger cortical capillary volume (median, 16.47 vs. 3.65, p<0.01), and a significantly larger cortical capillary total surface area (median, 7885.79 vs. 1957.16, p<0.01) compared with the NG group.ConclusionsThese data demonstrate that exercise improved spatial learning, memory capacity and cortical capillaries in aged rats.

Which facets of human spatial navigation do sex and menstrual cycle influence? To answer this question, a cross-sectional online study of reproductive age women and men was conducted in which participants were asked to demonstrate and self-report their spatial navigation skills and strategies. Participants self-reported their sex and current menstrual phase [early follicular (EF), late follicular/periovulatory (PO), and mid/late luteal (ML)], and completed a series of questionnaires and tasks measuring self-reported navigation strategy use, topographical memory, cognitive map formation, face recognition, and path integration. We found that sex influenced self-reported use of cognitive map- and scene-based strategies, face recognition, and path integration. Menstrual phase moderated the influence of sex: compared to men, women had better face recognition and worse path integration, but only during the PO phase; PO women were also better at path integration in the presence of a landmark compared to EF + ML women and men. These findings provide evidence that human spatial navigation varies with the menstrual cycle and suggest that sensitivity of the entorhinal cortex and longitudinal axis of the hippocampus to differential hormonal effects may account for this variation.

Influence of cognitive and motor tasks using smartphone during gait: EMG and gait performance analysis – Dual-task study