Solving small spaces: investigating the use of landmark cues in brown capuchins (Cebus apella)

Some researchers have recently argued that humans may be unusual among primates in preferring to use landmark information when reasoning about some kinds of spatial problems. Some have explained this phenomenon by positing that our species’ tendency to prefer landmarks stems from a human-unique trait: language. Here, we test this hypothesis—that preferring to use landmarks to solve such tasks is related to language ability—by exploring landmark use in a spatial task in one non-human primate, the brown capuchin monkey (Cebus apella). We presented our subjects with the rotational displacement task, in which subjects attempt to relocate a reward hidden within an array of hiding locations which are subsequently rotated to a new position. Over several experiments, we varied the availability and the salience of a landmark cue within the array. Specifically, we varied (1) visual access to the array during rotation, (2) the type of landmark, (3) the consistency of the landmark qualities, and (4) the amount of exposure to the landmark. Across Experiments 1 through 4, capuchins did not successfully use landmarks cues, suggesting that non-linguistic primates may not spontaneously use landmarks to solve some spatial problems, as in this case of a small-scale dynamic spatial task. Importantly, we also observed that capuchins demonstrated some capacity to learn to use landmarks in Experiment 4, suggesting that non-linguistic creatures may be able to use some landmarks cues in similar spatial tasks with extensive training.     

Wayfinding behavior and spatial knowledge of adults and children in a virtual environment: The role of landmarks

This study investigated the effect of different organizations of landmark-location pairings as fine-space information on wayfinding behavior and spatial knowledge on a total of 90 participants: 30 second graders, 30 sixth graders, and 30 adults. All participants had to find their way to a goal in a virtual environment with either randomized or categorical landmarks, or without any landmarks. Thereafter, they had to find the shortest way from the start position to the goal in two consecutive trials (wayfinding performance), and they had to solve a number of spatial knowledge tasks. The results showed that independent of their categorical function, the existence of landmarks influenced the way-finding performance of adults and children in the same way. Whereas the presence of landmarks had no effect on spatial survey knowledge, landmark knowledge itself was influenced by the categorical function of the landmarks presented. Moreover, second graders showed limited achievement compared to adults independent of the existence of landmarks. The main results implicate firstly that children at school age indeed are able to use landmark-location pairings as fine-space information like adults during learning an unknown environmental space, and secondly that a dissociation between wayfinding behavior and spatial knowledge might exist.     

Disorientation inhibits landmark use in 12-18-month-old infants

Recent research has indicated that, particularly under conditions of inertial disorientation, mammals may be sensitive to landmark configuration geometry at the expense of individual featural information when locating hidden goals. The current study sought to establish whether landmark use could be demonstrated in 12-18-month-old infants with and without a disorientation procedure, and with geometrically ambiguous landmark configurations. A peekaboo paradigm was employed in which infants learned to anticipate a peekaboo event after a cue from two locations within a circular arena, followed by a test trial from a novel position in which no peekaboo occurred after the cue. In all conditions, an isosceles triangle arrangement of landmarks was used, with peekaboo occurring between the landmarks of one of the two equal "sides", thus being geometrically ambiguous. In two conditions, the landmarks were distinctive, and in two further conditions, they were identical. In one of the distinctive conditions and one of the identical landmark conditions, infants underwent a disorientation procedure in between training and test trials. Only oriented infants with distinctive landmarks were successful in test trials, thus suggesting that infants are able to use the individual features of landmarks to locate a goal, but can only do so if oriented.     

Development of spatial memory and spatial orientation in preschoolers and primary school children

The present study addresses the question of what kind of information children use when orientating in new environments, if given proximal and distal landmarks, and how spatial memory develops in the investigated age groups. Ten 5-year-old, ten 7-year-old and ten 10-year-old children were presented with the ‘Kiel Locomotor Maze’, containing features of the Radial Arm Maze and the Morris Water Maze, in order to assess spatial memory and orientation. Children had to learn to approach baited locations only. Task difficulty was equated with respect to the children's age. Training was given until the children reached criterion. During testing, the maze configuration and response requirements were systematically altered, including response rotation, cue rotation, cue deletion and response rotation with cue deletion in order to assess the spatial strategies used by the children. During training and testing, working-memory errors (WM), reference-memory errors (RM) and working-reference memory errors (WR) were recorded. As expected, no difference between age groups appeared during training, thus confirming comparable task difficulty across age groups. During testing, age groups differed significantly with regard to the orientation strategy used. The 5-year-olds were bound to a cue strategy, orientating towards local, proximal cues. The 10-year-olds mastered all tasks, thus displaying a place strategy, being able to use distal cues for orientation, and were even able to do so after being rotated 180°. The 7-year-olds proved to be at an age of transition: five of them were bound to a cue strategy, five children were able to adopt a place strategy. The differences in the orientation strategies used by children of different age groups was reflected by the sum of errors they made, also by RM. WM were found to be rare, especially in older children. We conclude that preschoolers use a cue strategy, that the development of place strategies occurs during primary school age and seems to be complete by the age of 10 years.     

Multiple-landmark piloting in pigeons (Columba livia): landmark configuration as a discriminative cue

Using the landmark-transformation technique, researchers have shown that pigeons (Columba livia) tend to encode a goal location relative to 1 landmark, even when multiple landmarks are in the vicinity of the goal. The current experiments examined pigeons' ability to use configural information from a set of landmarks by making the arrangement of 4 landmarks a discriminative cue to the location of buried seeds. Results showed that pigeons used information from the 3 consistently placed landmarks to search accurately when 1 landmark was displaced. Findings indicate that pigeons are able to search for a goal using information from multiple landmarks instead of just 1 and that landmark use by these birds may be more flexible than previously theorized.     

Route navigating without place recognition: what is recognised in recognition-triggered responses?

The use of landmark information in a route-navigation task has been investigated in a virtual environment. After learning a route, subjects were released at intermediate points along the route and asked to indicate the next movement direction required to continue the route. At each decision point, three landmarks were present, one of which was viewed centrally and two which appeared in the periphery of the visual field when approaching the decision point. In the test phase, landmarks could be replaced either within or across places. If all landmarks combined into a new place had been associated with the same movement direction during training, subjects performed as in the control condition. This indicates that they did not need to recognise places as configurations of landmarks. If, however, landmarks that had been associated with conflicting movement directions during training were combined, subjects' performance was reduced. We conclude that local views and objects are recognised individually and that the associated directions are combined in a voting scheme. No evidence was found for a recognition of places as panoramic views or configurations of objects.     

Development of allocentric spatial recall from new viewpoints in virtual reality

Using landmarks and other scene features to recall locations from new viewpoints is a critical skill in spatial cognition. In an immersive virtual reality task, we asked children 3.5–4.5 years old to remember the location of a target using various cues. On some trials they could use information from their own self‐motion. On some trials they could use a view match. In the very hardest kind of trial, they were ‘teleported’ to a new viewpoint and could only use an allocentric spatial representation. This approach provides a strict test for allocentric coding (without either a matching viewpoint or self‐motion information) while avoiding additional task demands in previous studies (it does not require them to deal with a small table‐top environment or to manage stronger cue conflicts). Both the younger and older groups were able to point back at the target location better than chance when they could use view matching and/or self‐motion, but allocentric recall was only seen in the older group (4.0–4.5). In addition, we only obtained evidence for a specific kind of allocentric recall in the older group: they tracked one major axis of the space significantly above chance, r(158) = .28, but not the other, r(158) = ?.01. We conclude that there is a major qualitative change in coding for spatial recall around the fourth birthday, potentially followed by further development towards fully flexible recall from new viewpoints.     

Orientation in the cuttlefish <Emphasis Type="Italic">Sepia officinalis</Emphasis>: response <Emphasis Type="Italic">versus</Emphasis> place learning

Several studies have demonstrated that mammals, birds and fish use comparable spatial learning strategies. Unfortunately, except in insects, few studies have investigated spatial learning mechanisms in invertebrates. Our study aimed to identify the strategies used by cuttlefish (Sepia officinalis) to solve a spatial task commonly used with vertebrates. A new spatial learning procedure using a T-maze was designed. In this maze, the cuttlefish learned how to enter a dark and sandy compartment. A preliminary test confirmed that individual cuttlefish showed an untrained side-turning preference (preference for turning right or left) in the T-maze. This preference could be reliably detected in a single probe trial. In the following two experiments, each individual was trained to enter the compartment opposite to its side-turning preference. In Experiment 1, distal visual cues were provided around the maze. In Experiment 2, the T-maze was surrounded by curtains and two proximal visual cues were provided above the apparatus. In both experiments, after acquisition, strategies used by cuttlefish to orient in the T-maze were tested by creating a conflict between the formerly rewarded algorithmic behaviour (turn, response learning) and the visual cues identifying the goal (place learning). Most cuttlefish relied on response learning in Experiment 1; the two strategies were used equally often in Experiment 2. In these experiments, the salience of cues provided during the experiment determined whether cuttlefish used response or place learning to solve this spatial task. Our study demonstrates for the first time the presence of multiple spatial strategies in cuttlefish that appear to closely parallel those described in vertebrates.     

The development of spatial location coding: Place learning and dead reckoning in the second and third years

There are two possible ways to code spatial location: viewer-referenced and externally referenced systems. The mature form of each system makes use of metric information (in forms of coding termed dead reckoning and place learning, respectively). Each system also exists in a simpler form not using metric information (termed response learning and cue learning, respectively). We report an experiment designed to examine the development of the two mature forms of spatial coding. Children aged 16 to 36 months were asked to search for objects hidden in a long rectangular sandbox, after they moved to the opposite side of the box, either with visual landmarks available or in a curtained environment. When moving in a curtained environment, and hence needing to rely primarily on dead reckoning, children across this age range performed at levels above chance but reliably less accurate than when they did not move. The size of the decrement due to movement did not decrease with age. Thus, the dead reckoning system may become available before 16 months but undergo no further improvement through 3 years. On the other hand, comparisons between children who moved in the curtained environment and children who moved with visual landmarks available showed that only children older than 21 months did better when external landmarks could be seen. This finding suggests a relatively late emergence of place learning.     

Multiple cue use and integration in pigeons (<Emphasis Type="Italic">Columba livia</Emphasis>)

Encoding multiple cues can improve the accuracy and reliability of navigation and goal localization. Problems may arise, however, if one cue is displaced and provides information which conflicts with other cues. Here we investigated how pigeons cope with cue conflict by training them to locate a goal relative to two landmarks and then varying the amount of conflict between the landmarks. When the amount of conflict was small, pigeons tended to integrate both cues in their search patterns. When the amount of conflict was large, however, pigeons used information from both cues independently. This context-dependent strategy for resolving spatial cue conflict agrees with Bayes optimal calculations for using information from multiple sources.     

The effect of experience on children's ability to show response and place learning

From a developmental perspective, it has been reasoned that over the course of development children make differential use of available landmarks in the surroundings to orient in space. The present study examined whether children can learn to apply different spatial strategies, focusing on different landmark cues. Children aged 7 and 10 years were tested on an object‐location memory task in which they learned a location relative to a direct cue or to indirect cues. Both age groups performed equally well on the direct test condition. However, children 7 years of age had difficulties with orienting relative to the indirect landmarks. Interestingly, their performance increased significantly with more relevant experience. Different explanations for these findings are discussed.     

The role of visual and body movement information in infant search

Three experiments investigated the use of visual input and body movement input arising from movement through the world on spatial orientation. Infants between 9 1/2 and 18 months participated in a search task in which they searched for a toy hidden in 1 of 2 containers. Prior to beginning search, either the infants or the containers were rotated 180 degrees; these rotations occurred in a lit or dark environment. These experiments were distinguished by the environmental cues for object location; Experiment 1 used a position cue, Experiment 2 a color cue, and Experiment 3 both position and color cues. Accuracy was better in Experiments 2 and 3 than in Experiment 1. All studies found that search was best after infant movement in the light; all other conditions led to equivalently worse performance. These results are discussed relative to a theoretical characterization of spatial coding focusing on the uses of spatial information.     

4-6岁儿童在小模型旋转任务中的线索学习与位置学习*

以90名4-6岁儿童为被试,探讨了儿童在小模型旋转任务中利用线索学习和位置学习表征空间位置的年龄特点。研究结果表明:(1)儿童对线索学习的利用要优于对位置学习的利用;(2)4岁儿童已经可以使用线索学习的方式表征空间位置,但到6岁左右才开始能够使用基于方向的位置学习;(3)线索特征对于儿童的线索学习有显著影响,明显、突出的线索有利于儿童的线索学习。     

Indirect landmark use at 6 months of age in a spatial orientation task

It was hypothesized that 6-month-old infants may be able to use indirect landmarks to locate a goal if (a) the landmarks are sufficiently distinctive and (b) the goal location is between landmarks, rather than on the opposite side of the space as was used in earlier research. Six-month-old infants were tested in a peekaboo paradigm in which they had to turn to a target location after displacement to a novel position. Infants looked to the goal location significantly more in a beacon and an indirect landmarks condition relative to a control and a single landmark condition. These results are discussed in terms of current theories of spatial development.     

Flexible learning and use of multiple-landmark information by pigeons (Columba livia) in a touch screen-based goal searching task

Three touch screen-based experiments were conducted to investigate whether pigeons would learn to use configural information about a goal's location in relation to a multiple-landmark array. In Experiment 1, 4 pigeons (Columba livia) were trained to peck a computer monitor at a location that constituted the third vertex of a hypothetical triangle defined by 2 different landmarks. The landmarks appeared in 3 orientations during the training, and the pigeons' goal-searching ability easily transferred to the landmarks presented in 3 novel orientations. Each landmark was asymmetric, so we next examined whether the pigeons used (a) the small-scale, local orientation information that could be inferred from each landmark individually, or (b) the large-scale, configural information that could be inferred from the spatial arrangement of multiple landmarks taken as a whole. Even when each single landmark appeared by itself, the pigeons were able to locate the goal accurately, suggesting that the large-scale, configural information was not essential. However, when 1 landmark locally pointed to a location that was consistent with the triangular configuration and the other landmark locally pointed to a different location, the pigeons predominantly pecked at the configurally array-consistent location. These results suggest that the pigeons redundantly learned both the large-scale, configural strategy and the local, single-landmark strategy, but they mainly used the latter information, and used the former information solely to disambiguate conflicts when the 2 landmarks pointed toward different targets. Such flexible learning and use of redundant information may reflect the pigeons' adaptation to unstable wild environments during their evolutionary history.     

Colour cues or spatial cues? Context-dependent preferences in the European greenfinch (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

Using featural cues such as colour to identify ephemeral food can increase foraging efficiency. Featural cues may change over time however; therefore, animals should use spatial cues to relocate food that occurs in a temporally stable position. We tested this hypothesis by measuring the cue preferences of captive greenfinches Carduelis chloris when relocating food hidden in a foraging tray. In these standardised associative learning trials, greenfinches favoured colour cues when returning to a foraging context that they had encountered before only once (“one-trial test”) but switched to spatial cues when they had encountered that scenario on ten previous occasions (“repeated-trial test”). We suggest that repeated encounters generated a context in which individuals had a prior expectation of temporal stability, and hence context-dependent cue selection. Next, we trained birds to find food in the absence of colour cues but tested them in the presence of visual distracters. Birds were able to learn spatial cues after one encounter, but only when visual distracters were identical in colouration. When a colourful distracter was present in the test phase, cue selection was random. Unlike the first one-trial test, birds were not biased towards this colourful visual distracter. Together, these results suggest that greenfinches are able to learn both cue types, colour cue biases represent learning, not simply distraction, and spatial cues are favoured over colour cues only in temporally stable contexts.     

Eye tracking, strategies, and sex differences in virtual navigation

Reports of sex differences in wayfinding have typically used paradigms sensitive to the female advantage (navigation by landmarks) or sensitive to the male advantage (navigation by cardinal directions, Euclidian coordinates, environmental geometry, and absolute distances). The current virtual navigation paradigm allowed both men and women an equal advantage. We studied sex differences by systematically varying the number of landmarks. Eye tracking was used to quantify sex differences in landmark utilisation as participants solved an eight-arm radial maze task within different virtual environments. To solve the task, participants were required to remember the locations of target objects within environments containing 0, 2, 4, 6, or 8 landmarks. We found that, as the number of landmarks available in the environment increases, the proportion of time men and women spend looking at landmarks and the number of landmarks they use to find their way increases. Eye tracking confirmed that women rely more on landmarks to navigate, although landmark fixations were also associated with an increase in task completion time. Sex differences in navigational behaviour occurred only in environments devoid of landmarks and disappeared in environments containing multiple landmarks. Moreover, women showed sustained landmark-oriented gaze, while men's decreased over time. Finally, we found that men and women use spatial and response strategies to the same extent. Together, these results shed new light on the discrepancy in landmark utilisation between men and women and help explain the differences in navigational behaviour previously reported.     

Sex differences and the effect of instruction on reorientation abilities by humans

This study examined whether differences in the amount of information provided to men and women, in the form of verbal instruction, influenced their encoding during a reorientation task. When a navigator needs to orient, featural (e.g., colour or texture) and geometry (e.g., metric information) are used to determine which direction to begin traveling. The current study used a spatial reorientation task to examine how men and women use featural and geometric cues and whether the content of the task’s instructions influenced how these cues were used. Participants were trained to find a target location in a rectangular room with distinctive objects situated at each corner. Once the participants were accurately locating the target, various tests manipulating the spatial information were conducted. We found both men and women encoded the featural cues, and even though the features provided reliable information, participants generally showed an encoding of geometry. However, when participants were not provided with any information about the spatial aspects of the task in the instructions, they failed to encode geometry. We also found that women used distant featural cues as landmarks when the featural cue closest to the target was removed, whereas men did not. Yet, when the two types of cues were placed in conflict, both sexes weighed featural cues more heavily than geometric cues. The content of the task instructions also influenced how cues were relied upon in this conflict situation. Our results have important implications for our understanding of how spatial cues are used for reorientation.     

Octopuses (Octopus bimaculoides) and cuttlefishes (Sepia pharaonis, S. officinalis) can conditionally discriminate

In complex navigation using landmarks, an animal must discriminate between potential cues and show context (condition) sensitivity. Such conditional discrimination is considered a form of complex learning and has been associated primarily with vertebrates. We tested the hypothesis that octopuses and cuttlefish are capable of conditional discrimination. Subjects were trained in two maze configurations (the conditions) in which they were required to select one of two particular escape routes within each maze (the discrimination). Conditional discrimination could be demonstrated by selecting the correct escape route in each maze. Six of ten mud-flat octopuses (Octopus bimaculoides), 6 of 13 pharaoh cuttlefish (Sepia pharaonis), and one of four common cuttlefish (S. officinalis) demonstrated conditional discrimination by successfully solving both mazes. These experiments demonstrate that cephalopods are capable of conditional discrimination and extend the limits of invertebrate complex learning.     

Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study

Hippocampal (HF)-lesioned pigeons display impaired homing ability when flying over familiar terrain, where they are presumably relying on a map-like representation of familiar landmarks to navigate. However, research carried out in the field precludes a direct test of whether hippocampal lesions compromise the ability of homing pigeons to navigate by familiar landmarks. To examine more thoroughly the relationship between hippocampus and landmark spatial learning, control, neostriatum-lesioned, and HF-lesioned homing pigeons were trained on two open field, laboratory, conditional discrimination tasks. One was a visual landmark array task, and the other was a room color discrimination task. For the tasks, the correct of three differently colored food bowls was determined by the spatial relationship among a group of five landmarks and room color, respectively. Intact control birds successfully learned both tasks, while neostriatum-lesioned birds successfully learned the landmark array task-the only task on which they were trained. By contrast, HF-lesioned birds successfully learned the room color task but were unable to learn the landmark array task. The data support the hypothesis that homing performance deficits observed in the field following hippocampal lesions are in part a consequence of an impairment in the ability of lesioned pigeons to use familiar visual landmarks for navigation.