Route sequence knowledge supports the formation of cognitive maps.

In this study, we examined the extent to which knowledge about the sequence of places encountered during route learning supports the formation of a metric cognitive map. In a between subjects design, participants learned a route until they could navigate it independently without error whilst also learning information about either the identity of places along the route (Recognition Learning condition) or the sequence of places along the route (Sequence Learning condition). In a follow-up Reconstruction of Order Task, we confirmed that participants in the Sequence Learning condition had more accurate route sequence knowledge than those in the Recognition Learning condition, despite requiring the same overall number of trials to learn the route. Participants then completed a Pointing Task to assess the quality of their cognitive map of the environment. Both groups performed above chance level, showing incidental encoding of metric information, but the Sequence Learning group produced significantly lower pointing errors than the Recognition Learning group. Further, we found that route distance between pairs of places was a strong predictor of pointing error in both groups, whilst Euclidean distance between places was a significant, but weak, predictor only for the Sequence Learning condition. The results of this study demonstrate that discrete route sequence knowledge directly supports the formation of metric cognitive maps. We consider how the results are best explained by interactions between striatal route representations and hippocampal metric representations, centered around the sequence of places acting as a scaffold for the encoding of metric information.

Associations of environmental and lifestyle factors with spatial navigation in younger and older adults.

OBJECTIVE: Advanced age is associated with prominent impairment in allocentric navigation dependent on the hippocampus. This study examined whether age-related impairment in allocentric navigation and strategy selection was associated with sleep disruption or circadian rest-activity fragmentation. Further, we examined whether associations with navigation were moderated by perceived stress and physical activity. METHOD: Sleep fragmentation and total sleep time over the course of 1 week were assayed in younger (n = 42) and older (n = 37) adults via wrist actigraphy. Subsequently, participants completed cognitive mapping and route learning tasks, as well a measure of spontaneous navigation strategy selection. Measurements of perceived stress and an actigraphy-based index of physical activity were also obtained. Circadian rest-activity fragmentation was estimated via actigraphy post-hoc. RESULTS: Age was associated with reduced cognitive mapping, route learning, allocentric strategy use, and total sleep time (ps < .01), replicating prior findings. Novel findings included that sleep fragmentation increased with advancing age (p = .009) and was associated with lower cognitive mapping (p = .022) within the older adult cohort. Total sleep time was not linearly associated with the navigation tasks (ps > .087). Post-hoc analyses revealed that circadian rest-activity fragmentation increased with advancing age within the older adults (p = .026) and was associated with lower cognitive mapping across the lifespan (p = .001) and within older adults (p = .005). Neither stress nor physical activity were robust moderators of sleep fragmentation associations with the navigation tasks (ps > .113). CONCLUSION: Sleep fragmentation and circadian rest-activity fragmentation are potential contributing factors to age effects on cognitive mapping within older adults.

Wood ants learn the magnetic direction of a route but express uncertainty because of competing directional cues.

Wood ants were trained indoors to follow a magnetically specified route that went from the centre of an arena to a drop of sucrose at the edge. The arena, placed in a white cylinder, was in the centre of a 3D coil system generating an inclined Earth-strength magnetic field in any horizontal direction. The specified direction was rotated between each trial. The ants' knowledge of the route was tested in trials without food. Tests given early in the day, before any training, show that ants remember the magnetic route direction overnight. During the first 2 s of a test, ants mostly faced in the specified direction, but thereafter were often misdirected, with a tendency to face briefly in the opposite direction. Uncertainty about the correct path to take may stem in part from competing directional cues linked to the room. In addition to facing along the route, there is evidence that ants develop magnetically directed home and food vectors dependent upon path integration. A second experiment asked whether ants can use magnetic information contextually. In contrast to honeybees given a similar task, ants failed this test. Overall, we conclude that magnetic directional cues can be sufficient for route learning.

Supporting route learning in older adults: the role of imagery strategy.

OBJECTIVES: Route learning is an everyday spatial ability important to individuals' independent living, and is known to decline with age. This study aimed to investigate the benefit of using an imagery strategy to support route learning in young and older adults. METHODS: Forty young adults and 40 older adults learned a path from a video. Twenty of each age group were taught to use an imagery strategy (strategy groups [SGs]), while the others received no specific instructions (control groups [CGs]). Then participants were asked to recall the order and location of landmarks they had seen along the path (landmark ordering and locating tasks). RESULTS: Young adults recalled the order and location of landmarks better than older adults, and the SGs outperformed the CGs regardless of age. The Age group x Learning group interaction was only significant for the landmark locating task, with the young CG performing better than the older CG, while the older SG proved as good at recalling landmark locations as the young SG. Further, it was only among the older adults that the SG outperformed the CG. CONCLUSION: These findings newly suggest that using imagery helps to sustain older adults' route learning ability, especially in spatial recall tasks demanding the active manipulation of spatial information learnt, such as locating landmarks previously encountered while navigating a path. These results are discussed within the aging and spatial cognition frameworks.

Multi-modal cue integration in the black garden ant.

In a constantly changing environment, it is advantageous for animals to encode a location (such as a food source) relying on more than one single cue. A certain position might, in fact, be signalled by the presence of information acquired through different sensory modalities which may be integrated into cohesive memories. Here, we aimed to investigate multi-sensory learning capabilities and multi-modal information integration in Lasius niger ants. Individual ants were placed in a Y-maze where odour information always led to a food reward; moreover, arm and wall colour were also predictive but only when co-occurring with odour in a specific combination. At test, the odour cue was made uninformative (it was present in both arms). Ants were still able to correctly locate the reward by integrating odour with the right colour and side combination. In a second experiment, we tested whether multi-modal cue integration can take place in a single trial. To this end, ants were exposed to a rewarded odour in a single-arm maze and could experience the Y-maze (with all available cues) only once. At test (which was identical to that of Experiment 1), ants showed a slight preference for the correct colour-side combination, although not significantly different from chance level. Our results showed the capability of black garden ants to code apparently redundant contextual information and to create and rely on conditional relationships between the information available. We argue that future studies should deepen the inquiry on the timing and progression of multi-modal cue learning.

A novel virtual-reality-based route-learning test suite: Assessing the effects of cognitive aging on navigation.

Most research groups studying human navigational behavior with virtual environment (VE) technology develop their own tasks and protocols. This makes it difficult to compare results between groups and to create normative data sets for any specific navigational task. Such norms, however, are prerequisites for the use of navigation assessments as diagnostic tools-for example, to support the early and differential diagnosis of atypical aging. Here we start addressing these problems by presenting and evaluating a new navigation test suite that we make freely available to other researchers (https://osf.io/mx52y/). Specifically, we designed three navigational tasks, which are adaptations of earlier published tasks used to study the effects of typical and atypical aging on navigation: a route-repetition task that can be solved using egocentric navigation strategies, and route-retracing and directional-approach tasks that both require allocentric spatial processing. Despite introducing a number of changes to the original tasks to make them look more realistic and ecologically valid, and therefore easy to explain to people unfamiliar with a VE or who have cognitive impairments, we replicated the findings from the original studies. Specifically, we found general age-related declines in navigation performance and additional specific difficulties in tasks that required allocentric processes. These findings demonstrate that our new tasks have task demands similar to those of the original tasks, and are thus suited to be used more widely.

Private information conflict: Lasius niger ants prefer olfactory cues to route memory.

Foraging animals use a variety of information sources to navigate, such as memorised views or odours associated with a goal. Animals frequently use different information sources concurrently, to increase navigation accuracy or reliability. While much research has focussed on conflicts between individually learned (private) information and social information, conflicts between private information sources have been less broadly studied. Here, we investigate such a conflict by pitting route memory against associative odour cue learning in the ant Lasius niger. Ants were alternatingly trained to find a high-quality scented food source on one arm of a Y-maze, and a differently scented low-quality food source on the opposite arm. After training, ants were presented with a Y-maze in which the high- and low-quality-associated scents were presented on opposite arms than during training. The ants showed an extremely strong preferential reliance on the odour cues, with 100% of ants following the high-quality odour and thus moving towards the side associated with low-quality food. Further experiments demonstrated that ants also learn odour associations more rapidly, requiring only one visit to each odour-quality combination to form a reliable association. Side associations in the absence of odours, by contrast, required at least two visits to each side for reliable learning. While much attention has been focussed on visual route learning in insect navigation and decision-making, our results highlight the overwhelming importance of odour cues in insect path choice.

Variations on a theme: bumblebee learning flights from the nest and from flowers.

On leaving a significant place to which they will return, bees and wasps perform learning flights to acquire visual information to guide them back. The flights are set in different contexts, such as from their nest or a flower, which are functionally and visually different. The permanent and inconspicuous nest hole of a bumblebee worker is locatable primarily through nearby visual features, whereas a more transient flower advertises itself by its colour and shape. We compared the learning flights of bumblebees leaving their nest or a flower in an experimental situation in which the nest hole, flower and their surroundings were visually similar. Consequently, differences in learning flights could be attributed to the bee's internal state when leaving the nest or flower rather than to the visual scene. Flights at the flower were a quarter as long as those at the nest and more focused on the flower than its surroundings. Flights at the nest covered a larger area with the bees surveying a wider range of directions. For the initial third of the learning flight, bees kept within about 5 cm of the flower and nest hole, and tended to face and fixate the nest, flower and nearby visual features. The pattern of these fixations varied between nest and flower, and these differences were reflected in the bees' return flights to the nest and flower. Together, these findings suggest that learning flights are tuned to the bees' inherent expectations of the visual and functional properties of nests and flowers.

Using virtual environments to investigate wayfinding in 8- to 12-year-olds and adults.

Wayfinding is the ability to learn and recall a route through an environment. Theories of wayfinding suggest that for children to learn a route successfully, they must have repeated experience of it, but in this experiment we investigated whether children could learn a route after only a single experience of the route. A total of 80 participants from the United Kingdom in four groups of 20 8-year-olds, 10-year-olds, 12-year-olds, and adults were shown a route through a 12-turn maze in a virtual environment. At each junction, there was a unique object that could be used as a landmark. Participants were "walked" along the route just once (without any verbal prompts) and then were asked to retrace the route from the start without any help. Nearly three quarters of the 12-year-olds, half of the 10-year-olds, and a third of the 8-year-olds retraced the route without any errors the first time they traveled it on their own. This finding suggests that many young children can learn routes, even with as many as 12 turns, very quickly and without the need for repeated experience. The implications for theories of wayfinding that emphasize the need for extensive experience are discussed.

How do we get there? Effects of cognitive aging on route memory.

Research into the effects of cognitive aging on route navigation usually focuses on differences in learning performance. In contrast, we investigated age-related differences in route knowledge after successful route learning. One young and two groups of older adults categorized using different cut-off scores on the Montreal Cognitive Assessment (MoCA), were trained until they could correctly recall short routes. During the test phase, they were asked to recall the sequence in which landmarks were encountered (Landmark Sequence Task), the sequence of turns (Direction Sequence Task), the direction of turn at each landmark (Landmark Direction Task), and to identify the learned routes from a map perspective (Perspective Taking Task). Comparing the young participant group with the older group that scored high on the MoCA, we found effects of typical aging in learning performance and in the Direction Sequence Task. Comparing the two older groups, we found effects of early signs of atypical aging in the Landmark Direction and the Perspective Taking Tasks. We found no differences between groups in the Landmark Sequence Task. Given that participants were able to recall routes after training, these results suggest that typical and early signs of atypical aging result in differential memory deficits for aspects of route knowledge.

Homing pigeons (Columba livia) modulate wingbeat characteristics as a function of route familiarity.

Mechanisms of avian navigation have received considerable attention, but whether different navigational strategies are accompanied by different flight characteristics is unknown. Managing energy expenditure is critical for survival; therefore, understanding how flight characteristics, and hence energy allocation, potentially change with birds' familiarity with a navigational task could provide key insights into the costs of orientation. We addressed this question by examining changes in the wingbeat characteristics and airspeed of homing pigeons (Columba livia) as they learned a homing task. Twenty-one pigeons were released 20 times individually either 3.85 or 7.06 km from home. Birds were equipped with 5 Hz GPS trackers and 200 Hz tri-axial accelerometers. We found that, as the birds' route efficiency increased during the first six releases, their median peak-to-peak dorsal body (DB) acceleration and median DB amplitude also increased. This, in turn, led to higher airspeeds, suggesting that birds fly slower when traversing unfamiliar terrain. By contrast, after route efficiency stabilised, birds exhibited increasing wingbeat frequencies, which did not result in further increases in speed. Overall, higher wind support was also associated with lower wingbeat frequencies and increased DB amplitude. Our study suggests that the cost of early flights from an unfamiliar location may be higher than subsequent flights because of both inefficient routes (increased distance) and lower airspeeds (increased time). Furthermore, the results indicate, for the first time, that birds modulate their wingbeat characteristics as a function of navigational knowledge, and suggest that flight characteristics may be used as 'signatures' of birds' route familiarity.

How to enhance route learning and visuo-spatial working memory in aging: a training for residential care home residents.

OBJECTIVES: This study aimed to assess the efficacy of a route-learning training in a group of older adults living in a residential care home. We verified the presence of training-specific effects in tasks similar to those trained - route-learning tasks - as well as transfer effects on related cognitive processes - visuo-spatial short-term memory (VSSTM; Corsi Blocks Test (CBT), forward version), visuo-spatial working memory (VSWM; CBT, backward version; Pathway Span Tasks; Jigsaw Puzzle Test) - and in self-report measures. The maintenance of training benefits was examined after 3 months. METHOD: Thirty 70-90-year-old residential care home residents were randomly assigned to the route-learning training group or to an active control group (involved in non-visuo-spatial activities). RESULTS: The trained group performed better than the control group in the route-learning tasks, retaining this benefit 3 months later. Immediate transfer effects were also seen in visuo-spatial span tasks (i.e., CBT forward and backward version and Pathway Span Task); these benefits had been substantially maintained at the 3-month follow-up. CONCLUSION: These findings suggest that a training on route learning is a promising approach to sustain older adults' environmental learning and some related abilities (e.g., VSSTM and VSWM), even in residential care home residents.

Evidence of trapline foraging in honeybees.

Central-place foragers exploiting floral resources often use multi-destination routes (traplines) to maximise their foraging efficiency. Recent studies on bumblebees have showed how solitary foragers can learn traplines, minimising travel costs between multiple replenishing feeding locations. Here we demonstrate a similar routing strategy in the honeybee (Apis mellifera), a major pollinator known to recruit nestmates to discovered food resources. Individual honeybees trained to collect sucrose solution from four artificial flowers arranged within 10 m of the hive location developed repeatable visitation sequences both in the laboratory and in the field. A 10-fold increase of between-flower distances considerably intensified this routing behaviour, with bees establishing more stable and more efficient routes at larger spatial scales. In these advanced social insects, trapline foraging may complement cooperative foraging for exploiting food resources near the hive (where dance recruitment is not used) or when resources are not large enough to sustain multiple foragers at once.

Asymmetric visual input and route recapitulation in homing pigeons.

Pigeons (Columba livia) display reliable homing behaviour, but their homing routes from familiar release points are individually idiosyncratic and tightly recapitulated, suggesting that learning plays a role in route establishment. In light of the fact that routes are learned, and that both ascending and descending visual pathways share visual inputs from each eye asymmetrically to the brain hemispheres, we investigated how information from each eye contributes to route establishment, and how information input is shared between left and right neural systems. Using on-board global positioning system loggers, we tested 12 pigeons' route fidelity when switching from learning a route with one eye to homing with the other, and back, in an A-B-A design. Two groups of birds, trained first with the left or first with the right eye, formed new idiosyncratic routes after switching eyes, but those that flew first with the left eye formed these routes nearer to their original routes. This confirms that vision plays a major role in homing from familiar sites and exposes a behavioural consequence of neuroanatomical asymmetry whose ontogeny is better understood than its functional significance.

Learning multiple routes in homing pigeons.

The aerial lifestyle of central-place foraging birds allows wide-ranging movements, raising fundamental questions about their remarkable navigation and memory systems. For example, we know that pigeons (Columba livia), long-standing models for avian navigation, rely on individually distinct routes when homing from familiar sites. But it remains unknown how they cope with the task of learning several routes in parallel. Here, we examined how learning multiple routes influences homing in pigeons. We subjected groups of pigeons to different training protocols, defined by the sequence in which they were repeatedly released from three different sites, either sequentially, in rotation or randomly. We observed that pigeons from all groups successfully developed and applied memories of the different release sites (RSs), irrespective of the training protocol, and that learning several routes in parallel did not impair their capacity to quickly improve their homing efficiency over multiple releases. Our data also indicated that they coped with increasing RS uncertainty by adjusting both their initial behaviour upon release and subsequent homing efficiency. The results of our study broaden our understanding of avian route following and open new possibilities for studying learning and memory in free-flying animals.

Interplay of wayfinding strategies in route repetition and route retracing.

This study explores the interplay of navigation strategies in route repetition (repeating a recently travelled route) and route retracing (returning to the start location of a recently travelled route). Specifically, we investigated how sequence knowledge contributes to route repetition and retracing. In the learning phase, participants passively transported along a route. In the test phase, they were then asked to repeat or retrace the route. Decision points were either presented in an order coherent with the learning phase (from start to destination in route repetition, or from destination to start in route retracing), or in a randomised order. As expected, participants performed better in route repetition than in route retracing. Performance declined when intersections were presented in a randomised order indicating that sequence knowledge contributed to route repetition and route retracing. Presenting intersections in an order coherent with learning boosted performance specifically on the first part of the route during route repetition. This effect was not observed during route retracing. These results show that sequence knowledge is utilised differently during route repetition and retracing. We argue that participants use a "sequence of turns" strategy alongside associating landmarks with direction changes during route repetition, and that it is unlikely that route retracing relies on the same type of sequence knowledge. Instead, we believe route retracing utilises knowledge about the sequence in which decision points are encountered. Overall, the findings highlight a complex interplay of different strategies in route repetition and retracing, shedding light on how navigators utilise sequence knowledge for effective navigation.

The impact of transcranial direct current stimulation combined with interim testing on spatial route learning in patients with schizophrenia.

BACKGROUND: Cognitive deficits in patients with schizophrenia have drawn widespread attention. Transcranial direct current stimulation (tDCS) can modulate cognitive processes by altering neuronal excitability. Previous studies have found that interim testing can enhance spatial route learning and memory in patients with schizophrenia. However, there has been limited research on the combined effects of these two methods on spatial route learning in these patients. OBJECTIVE: To investigate whether the combination of tDCS and interim testing can effectively contribute to the maintenance of spatial route memory in patients with schizophrenia. The study involved conducting route learning using interim testing after anodal tDCS treatment on the left dorsolateral prefrontal cortex (L-DLPFC). METHODS: Ninety-two patients with schizophrenia were recruited and divided into groups receiving anodal, sham, or no stimulation. The anodal group received L-DLPFC tDCS treatment 10 times over 5 days (twice daily for 20 min). After treatment, spatial route learning was assessed in interim testing. Correct recall rates of landmark positions and proactive interference from prior learning were compared among the groups. RESULTS: Regardless of stimulation type, the interim testing group outperformed the relearning group. Additionally, recall scores were higher following anodal stimulation, indicating the efficacy of tDCS. CONCLUSIONS: Both tDCS and interim testing independently enhance the ability to learn new information in spatial route learning for patients with schizophrenia, indicating that tDCS of the left DLPFC significantly improves memory in these patients.

Landmark Sequence Learning from Real-World Route Navigation and the Impact of Navigation Aid Visualisation Style.

Primacy and recency features of serial memory are a hallmark of typical memory functions that have been observed for a wide array of tasks. Recently, the ubiquity of this serial position effect has been supported for objects learned during navigation, with canonical serial position functions observed for sequence memory of landmarks that were encountered along a route during a highly controlled virtual navigation task. In the present study, we extended those findings to a real-world navigation task in which participants actively walked a route through a city whilst using a navigation aid featuring either realistic or abstract landmark visualisation styles. Analyses of serial position functions (i.e., absolute sequence knowledge) and sequence lags (i.e., relative sequence knowledge) yielded similar profiles to those observed in a lab based virtual navigation task from previous work and non-spatial list learning studies. There were strong primacy effects for serial position memory in both conditions; recency effects only in the realistic visualisation condition; a non-uniform distribution of item-lags peaking at lag +1; and an overall bias towards positive lags for both visualisation conditions. The findings demonstrate that benchmark serial position memory effects can be observed in uncontrolled, real-world behaviour. In a navigation context, the results support the notion that general memory mechanisms are involved in spatial learning, and that landmark sequence knowledge is a feature of spatial knowledge which is affected by navigation aids.

Testing landmark-specific effects on route navigation in an ecologically valid setting: a simulated driving study.

We used a driving simulator to investigate landmark-based route navigation in young adults. Previous research has examined how proximal and distal landmarks influence route navigation, however, these effects have not been extensively tested in ecologically-relevant settings. We used a virtual town in which participants learned various routes while simultaneously driving. We first examined the effect of four different landmark conditions on navigation performance, such that each driver experienced one of four versions of the town with either proximal landmarks only, distal landmarks only, both proximal and distal landmarks, or no landmarks. Drivers were given real-time navigation directions along a route to a target destination, and were then tested on their ability to navigate to the same destination without directions. We found that the presence of proximal landmarks significantly improved route navigation. We then examined the effect of prior exposure to proximal vs. distal landmarks by testing the same drivers in the same environment they previously encountered, but with the landmarks removed. In this case, we found that prior exposure to distal landmarks significantly improved route navigation. The present results are in line with existing research on route navigation and landmarks, suggesting that these findings can be extended to ecologically-relevant settings.

Spatial navigation in older adults with mild cognitive impairment and dementia: A systematic review and meta-analysis.

In this systematic review and meta-analysis, we compared the spatial navigation performance of older adults with mild cognitive impairment (MCI), Alzheimer's Disease (AD), and other dementias, using healthy older adults as controls. In addition, we evaluated the possible influence of the environment type (virtual and real), protocol (object- or environment-based), and the navigation mode (active and passive navigation) on spatial navigation task performance. In total, 1372 articles were identified and 24 studies were included in the meta-analysis. We found a large effect size on the spatial navigation performance of patients with cognitive decline (standardized mean difference (SMD) = 0.87, confidence interval (CI95%) = 0.62-1.09, p < 0.001), especially amnestic MCI (SMD = 1.10, CI95% = 0.71-1.49, p < 0.001) and patients with AD (SMD = 1.60, CI95% = 1.25-1.95, p < 0.001). However, the tasks did not identify mixed and vascular dementia (SMD = 0.92, CI95% = -0.33-2.18, p = 0.15 and SMD = 0.65, CI95% = -0.67-1.97, p = 0.33, respectively). Spatial navigation ability assessed using the Floor Maze Test showed the largest effect size in differentiating healthy older adults and patients with cognitive decline (SMD = 1.98,CI95% = 1.00-2.97, p < 0.001). In addition, tasks that require walking showed the greatest differences between the two groups. These results suggest that spatial navigation impairment is important, but disease-specific behavioral biomarker of the dementia pathology process that can be identified even in the early stages.