Spatial behavior in male and female crayfish (Orconectes rusticus): learning strategies and memory duration

Previous studies have demonstrated that animals use multiple strategies to solve spatial tasks. We used a T-maze to examine spatial behavior in crayfish, using visual and tactile stimuli as place cues and a food-scented escape tank as reinforcement to leave the maze. In trials on a single day and across multiple days, crayfish learned to exit the maze with significantly reduced latency and with fewer turns. In addition, we examined place memory in 40-min periods with the maze closed and found that crayfish spent longer in the vicinity of a previously open exit compared to a closed exit. Probe tests were conducted using a forced-choice procedure to determine whether crayfish remembered the route out of the maze using primarily place cues or response learning. We found that approximately equal numbers of animals used each strategy, and individuals were able to switch from one strategy to the other on different test days. Males and females did not differ significantly in their performance in the place memory test, maze exit task, or probe tests. Both sexes displayed place memory for the exit location and reduced latency to exit during trials 24 h, 48 h, 72 h, and 1 week after initial training trials, suggesting that spatial memories in crayfish are relatively enduring.     

Beacon training in a water maze can facilitate and compete with subsequent room cue learning in rats

In Stage 1 of 4 experiments in which rats completed a water-maze blocking procedure, experimental groups were trained to use a predictive beacon (hanging above, connected to, or displaced from the platform) to find a submerged escape platform in the presence of predictive or irrelevant background cues and in the presence or absence of irrelevant landmarks. In Stage 2, a fixed beacon, landmarks, and background cues all predicted the platform location. A Room Test (landmarks and background cues only) showed that Stage 1 training with a fixed hanging beacon or the moving displaced beacon facilitated Stage 2 learning of predictive room cues for experimental relative to control subjects. In contrast, Stage 1 training with a moving pole beacon interfered with Stage 2 learning about predictive room cues relative to controls, whereas training with a fixed pole or moving hanging beacon had no effect. We conclude that multiple spatial learning processes influence locating an escape platform in the water maze.     

Not using the obvious: desert ants, Melophorus bagoti, learn local vectors but not beacons in an arena

Many ant species travel large distances to find food, sometimes covering distances that are up to one million times their body length. Even when these foraging trips follow convoluted paths, the ants usually find their way back to their nest with precision (Wehner et al. in J Exp Biol 199:129–140, 1996). Ants have been shown to use both compass cues in the sky (pattern of polarised light) and landmarks on Earth to return to their nest. We present two experiments conducted on a solitary foraging ant: Melophorus bagoti in their natural habitat in the central Australian desert. Ants were trained and tested in situ. We tested foragers’ ability to exit a circular arena which provided an undifferentiated panorama. Artificial visual landmarks were located near a small exit. On tests in which path integration information was not available, foragers did not use artificial landmarks as beacons. Instead, they oriented in the learned exit direction, whether or not it pointed to the nest. We suggest that M. bagoti foragers learned a context-specific local vector when cued by the context of the circular arena. Our findings present the first evidence that M. bagoti foragers learn context-specific compass directions to chart their initial path home.     

Exposure to Spatial Cues Facilitates Visual Discrimination but Not Spatial Guidance

The performance in a radial-arm maze of two groups of rats with restricted access to extra-maze visual cues was studied. One group received extensive exposure to the visual environment of the maze, whereas the second group was never exposed to the environment, aside from their experience in the maze itself. Spatial exposure resulted in a slightly improved ability to discriminate between previously visited and unvisited spatial locations, which can be explained on the basis of general perceptual learning processes. However, there was no evidence that spatial exposure resulted in control of choices by the spatial relations among the maze locations. These results are discussed in terms of theories of spatial learning which appeal to perceptual learning and cognitive mapping.     

Facilitation of learning spatial relations among locations by visual cues: generality across spatial configurations

Spatial pattern learning permits the learning of the location of objects in space relative to each other without reference to discrete visual landmarks or environmental geometry. In the present experiment, we investigated conditions that facilitate spatial pattern learning. Specifically, human participants searched in a real environment or interactive 3-D computer-generated virtual environment open-field search task for four hidden goal locations arranged in a diamond configuration located in a 5 × 5 matrix of raised bins. Participants were randomly assigned to one of three groups: Pattern Only, Landmark + Pattern, or Cues + Pattern. All participants experienced a Training phase followed by a Testing phase. Visual cues were coincident with the goal locations during Training only in the Cues + Pattern group whereas a single visual cue at a non-goal location maintained a consistent spatial relationship with the goal locations during Training only in the Landmark + Pattern group. All groups were then tested in the absence of visual cues. Results in both environments indicated that participants in all three groups learned the spatial configuration of goal locations. The presence of the visual cues during Training facilitated acquisition of the task for the Landmark + Pattern and Cues + Pattern groups compared to the Pattern Only group. During Testing the Landmark + Pattern and Cues + Pattern groups did not differ when their respective visual cues were removed. Furthermore, during Testing the performance of these two groups was superior to the Pattern Only group. Results generalize prior research to a different configuration of spatial locations, isolate spatial pattern learning as the process facilitated by visual cues, and indicate that the facilitation of learning spatial relations among locations by visual cues does not require coincident visual cues.     

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.     

Radial-arm-maze behavior of the red-footed tortoise (Geochelone carbonaria)

The radial-arm maze is an established method for testing an animal's spatial win-shift behavior. Research on mammals, birds, and fish has shown that the mastery of this task is commonly mediated, to different degrees, by two types of strategy: those based on external cues and those based on response stereotypy. In the present study we trained four red-footed tortoises (Geochelone carbonaria) to navigate an eight-arm radial maze while providing different levels of access to visual room cues. The results indicate that response stereotypy is the more prevalent mechanism in these tortoises, although navigation based on landmarks can also occur if learned initially. The findings suggest that tortoise spatial navigation may be more similar to that observed in mammals and birds than previously thought.     

Spatial relational memory in 9-month-old macaque monkeys

This experiment assesses spatial and nonspatial relational memory in freely moving 9-mo-old and adult (11-13-yr-old) macaque monkeys (Macaca mulatta). We tested the use of proximal landmarks, two different objects placed at the center of an open-field arena, as conditional cues allowing monkeys to predict the location of food rewards hidden in one of two sets of three distinct locations. Monkeys were tested in two different conditions: (1) when local visual cues marked the two sets of potentially baited locations, so that monkeys could use both local and spatial information to discriminate these locations from never-baited locations; and (2) when no local visual cues marked the two sets of potentially baited locations, so that monkeys had to rely on a spatial relational representation of the environment to discriminate these locations. No 9-mo-old or adult monkey associated the presence of the proximal landmarks, at the center of the arena, with the presence of food in one set of three distinct locations. All monkeys, however, discriminated the potentially baited locations in the presence of local visual cues, thus providing evidence of visual discrimination learning. More importantly, all 9-mo-old monkeys tested discriminated the potentially baited locations in absence of the local visual cues, thus exhibiting evidence of spatial relational learning. These findings indicate that spatial memory processes characterized by a relational representation of the environment are present as early as 9 mo of age in macaque monkeys.     

The role of the hippocampus in the retrieval of a spatial location

Based on computational models of the hippocampus, it has been suggested that a possible mechanism for memory retrieval is pattern completion, wherein an autoassociative network recalls previous patterns of activity given noisy or degraded cues. However, there are few behavioral data examining pattern completion per se in the hippocampus. Here, we present a study in which rats were tested on a spatial location retrieval paradigm, each trial of which consisted of a sample and choice phase. During the sample phase, rats were trained to displace an object in one of 15 possible locations to retrieve a food reward and return to the start-box on a cheeseboard maze. The object was then removed and the same location was re-baited for the choice phase. The rats' accuracy in returning to the correct location was recorded. On test trials, visual extramaze cues, vestibular cues, or both were manipulated to assess pattern completion in normal rats. Subjects were then randomly assigned to receive a cortical control, a sham, or a dorsal and ventral hippocampal lesion and were retested on the task. Control and unoperated rats were able to perform the task when visual extramaze or vestibular cues were reliable, but not when they were manipulated. Rats with hippocampal lesions were impaired in the baseline condition, as well as during all manipulations. These results support the hypothesis that the hippocampus supports the retrieval of a spatial location, possibly through a process of pattern completion.     

Spatial and nonspatial escape strategies in the Barnes maze

The Barnes maze is a spatial memory task that requires subjects to learn the position of a hole that can be used to escape the brightly lit, open surface of the maze. Two experiments assessed the relative importance of spatial (extra-maze) versus proximal visible cues in solving the maze. In Experiment 1, four groups of mice were trained either with or without a discrete visible cue marking the location of the escape hole, which was either in a fixed or variable location across trials. In Experiment 2, all mice were trained with the discrete visible cue marking the target hole location. Two groups were identical to the cued-target groups from Experiment 1, with either fixed or variable escape locations. For these mice, the discrete cue either was the sole predictor of the target location or was perfectly confounded with the spatial extra-maze cues. The third group also used a cued variable target, but a curtain was drawn around the maze to prevent the use of spatial cues to guide navigation. Probe trials with all escape holes blocked were conducted to dissociate the use of spatial and discrete proximal cues. We conclude that the Barnes maze can be solved efficiently using spatial, visual cue, or serial-search strategies. However, mice showed a strong preference for using the distal room cues, even when a discrete visible cue clearly marked the escape location. Importantly, these data show that the cued-target control version of the Barnes maze as typically conducted does not dissociate spatial from nonspatial abilities.     

Landmark Stability: Further Studies Pointing to a Role in Spatial Learning

Two experiments were conducted to investigate the possible role of landmark stability in spatial learning. Rats were trained to search in a large arena for food hidden at a consistent distance and direction from either a single radially symmetric landmark or an array of two landmarks. We varied the relative degree to which the landmark array and/or the cues of the training context predicted the location of food, without varying the conditional probability of food being available given either cue. Experiment 1 used vestibular disorientation to ensure control of search location by experimenter-controlled cues. The results showed that making either a single landmark or a cluster of two adjacent landmarks the sole spatial predictor of reward location reduced the accuracy of search compared to a condition where both the landmark array and context cues were reliable spatial predictors. Varying global landmark stability had no effect when training was conducted using an array of two landmarks located some distance from each other. Context cues, when tested alone, triggered very little searching in appropriate locations, and the absolute magnitude of control over search was insufficient to account for the superiority of stable landmarks. The better learning with a stable landmark, and the dependence of this effect on the geometrical arrangement of landmarks, points to the conditions of spatial learning involving additional principles to those of simple associative conditioning. Experiment 2 examined landmark stability using a single landmark and fixed directional cues in the absence of vestibular disorientation. This also revealed a relative advantage of landmark stability, but animals with a landmark that moved from trial to trial did show some evidence of learning. Context cues when tested alone had minimal influence. Parametric manipulation of landmark stability offers a novel way of influencing spatial learning and thus understanding better the process through which egocentric representations of perceived space are transformed into allocentric representations of the real world. The purpose of this paper is to describe two experiments concerned with identifying the psychological processes of allocentric spatial learning. The results point to the idea that landmark stability is an important factor in spatial learning. Specifically, they reveal that whether or not a landmark will be used for the purpose of representing the location of another object (including hidden objects) is influenced by whether it is perceived as geometrically stable with respect to at least one other landmark and/or certain geometric features of the environment. This phenomenon is relevant to the application of associative learning principles to the spatial domain.     

Optimal combination of environmental cues and path integration during navigation

Navigation is influenced by body-based self-motion cues that are integrated over time, in a process known as path integration, as well as by environmental cues such as landmarks and room shape. In two experiments we explored whether humans combine path integration and environmental cues (Exp. 1: room shape; Exp. 2: room shape, single landmark, and multiple landmarks) to reduce response variability when returning to a previously visited location. Participants walked an outbound path in an immersive virtual environment before attempting to return to the path origin. Path integration and an environmental cue were both available during the outbound path, but experimental manipulations created single- and dual-cue conditions during the return path. The response variance when returning to the path origin was reduced when both cues were available, consistent with optimal integration predicted on the basis of Bayesian principles. The findings indicate that humans optimally integrate multiple spatial cues during navigation. Additionally, a large (but not a small) cue conflict caused participants to assign a higher weight to path integration than to environmental cues, despite the relatively greater precision afforded by the environmental cues.     

Maze Learning by Honeybees

This study examines whether honeybees can learn to fly through complex mazes, in the presence or the absence of specific visual cues. The results are summarized as follows: 1. Bees can learn to fly through a complex maze by following a trail of colored marks. 2. Bees, initially trained to follow color marks through an initial part of the maze, are immediately able to use the same sign-tracking cue to find their way through the rest of the maze, which is unfamiliar to them. 3. Bees trained to follow color marks through a particular maze can use the same cue to negotiate a novel maze. 4. Bees trained to use a particular color to negotiate a maze can immediately use a novel color to negotiate the same maze or even a novel maze. 5. After learning to negotiate a maze by following colored marks, bees can find their way through the maze even when the marks are removed, albeit at reduced levels of accuracy. Thus, the trained bees do not rely solely on sign-tracking to find their way through the maze: they also acquire a spatial memory of the maze or at least a sequence of motor commands describing the correct path through it. 6. Bees can learn to use color as a signal even when it indicates the path through the maze in a symbolic way, for example, blue indicating a turn to the right and green a turn to the left. 7. Bees can learn an unmarked maze. Performance under these conditions is poorer than when marks are provided, but is still significantly better than chance level. 8. Control experiments rule out the use of external landmarks in all of these situations.     

Spatial learning in a T-maze by the crayfish Orconectes rusticus

The T-maze has commonly been used to investigate the mechanisms underlying spatial learning in vertebrates and has yielded much information about how animals use response and place cues to orient toward a goal. We designed a T-maze to study the spatial learning abilities of crayfish (Orconectes rusticus), using tactile stimuli as a place cue and escape from warm water for reinforcement. An initial experiment found that most animals did not display a side-turning bias when first placed in the maze, and hence animals were randomly assigned to escape from the left or the right arm, one of which contained a smooth floor and the other a rough floor. We found that, over repeated trials, the latency to escape and the number of turns made prior to escaping significantly decreased indicating that crayfish learned to escape from the maze more rapidly and efficiently. Learning occurred over the course of six trials on a single day, and over 5 days of testing, providing evidence for spatial memory lasting 24 hr. In probe trials, in which experienced animals started the maze in an arm opposite to that used during training trials, crayfish did not display a preference for either response-based learning or place-based learning. Instead they engaged in renewed exploration of the entire maze. These findings suggest that, in addition to remembering the location of the exit, crayfish also remembered the overall configuration of the maze.     

Win-shift and win-stay learning in the short-beaked echidna (<Emphasis Type="Italic">Tachyglossus aculeatus</Emphasis>)

Numerous previous investigators have explained species differences in spatial memory performance in terms of differences in foraging ecology. In three experiments we attempted to extend these findings by examining the extent to which the spatial memory performance of echidnas (or "spiny anteaters") can be understood in terms of the spatio-temporal distribution of their prey (ants and termites). This is a species and a foraging situation that have not been examined in this way before. Echidnas were better able to learn to avoid a previously rewarding location (to "win-shift") than to learn to return to a previously rewarding location (to "win-stay"), at short retention intervals, but were unable to learn either of these strategies at retention intervals of 90 min. The short retention interval results support the ecological hypothesis, but the long retention interval results do not. Electronic Publication     

The spatial distribution of inhibition of return

Inhibition of return (IOR) refers to the finding that response times (RTs) are typically slower for targets at previously attended (cued) locations than for targets at novel (uncued) locations. Although previous research has indicated that IOR may spread beyond a cued location, the present study is the first to examine the spatial distribution of IOR with high spatial resolution over a large portion of the central visual field. This was done by using a typical IOR procedure (cue, delay, target) with 4 cue locations and 441 target locations (each separated by 1° of visual angle). The results indicate that IOR spreads beyond the cued location to affect the cued hemifield. However, the cues also produced a gradient of RTs throughout the visual field, with inhibition in the cued hemifield gradually giving way to facilitation in the hemifield opposite the cue.     

Acute Ethanol Administration Impairs Spatial Performance While Facilitating Nonspatial Performance in Rats

Acute ethanol administration produces learning and memory impairments similar to those found following lesions to the hippocampal system in rats. For example, both ethanol and hippocampal lesions impair performance on spatial learning and memory tasks while sparing performance on many nonspatial learning and memory tasks. Lesions to the hippocampal system can also alter the nature of the information that the animal uses to guide its behavior, from using spatial information to using individual cues. In the present experiment, rats were trained, while sober, to navigate on an eight-arm radial arm maze to a specific arm for food reward. During training, the rewarded arm was always in the same specific location and contained well-defined cues. After the rat learned the task, a memory test was conducted under different doses of ethanol (0.0 g/kg [saline control], 1.0, 1.5, or 2.0 g/kg, intraperitoneal). On the test day the maze was rotated so that the cued arm was 90 degrees to the right of its original position. During testing, intact rats showed a significant bias to approach the place where they had been previously rewarded, even though the cue was no longer located there. Acute ethanol administration dose dependently reduced approaches to the rewarded place. However, ethanol administration did not result in increases in random choices; rather, it resulted in a dose-dependent increase in approaches to the cued arm, now in a new location. These results extend previous research showing that acute ethanol administration and lesions to the hippocampal system produce similar effects on learning and memory in rats.     

Significance of visual cues in choice behavior in the female zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis><Emphasis Type="Italic">castanotis</Emphasis>)

Female zebra finches show a preference for male zebra finches over heterospecific males based solely on the auditory cues of males, such as songs. The present study was designed to investigate whether females show a similar preference for male zebra finches based solely on visual cues. Using a Y-maze apparatus, social preference of female zebra finches was studied between male zebra finches and male Bengalese finches in three experiments. In experiment 1, where female zebra finches could see and hear live male zebra finches and male Bengalese finches, the females preferred to associate with the male zebra finches. In experiment 2, using a sound-attenuated experimental apparatus, subjects could see, but not hear, male zebra finches and male Bengalese finches. The subjects did not show a significant preference for associating with zebra finches. In experiment 3, as in experiment 2, females could see live male zebra finches and male Bengalese finches in the sound-attenuated chambers. However, in experiment 3, the subjects also heard prerecorded auditory cues (i.e., songs and calls) of male zebra finches, which were presented simultaneously in both arms of the maze. Although the females could not use the auditory cues to identify the location of the male zebra finches, they preferred to associate with the male zebra finches rather than the male Bengalese finches. These results suggest that visual cues alone were effective in initiating choice behaviors by females and that auditory cues facilitate such visually based choice behaviors. Electronic Publication     

Reorienting with terrain slope and landmarks

Orientation (or reorientation) is the first step in navigation, because establishing a spatial frame of reference is essential for a sense of location and heading direction. Recent research on nonhuman animals has revealed that the vertical component of an environment provides an important source of spatial information, in both terrestrial and aquatic settings. Nonetheless, humans show large individual and sex differences in the ability to use terrain slope for reorientation. To understand why some participants—mainly women—exhibit a difficulty with slope, we tested reorientation in a richer environment than had been used previously, including both a tilted floor and a set of distinct objects that could be used as landmarks. This environment allowed for the use of two different strategies for solving the task, one based on directional cues (slope gradient) and one based on positional cues (landmarks). Overall, rather than using both cues, participants tended to focus on just one. Although men and women did not differ significantly in their encoding of or reliance on the two strategies, men showed greater confidence in solving the reorientation task. These facts suggest that one possible cause of the female difficulty with slope might be a generally lower spatial confidence during reorientation.     

How rats perform spatial working memory tasks: Limitations in the use of egocentric and idiothetic working memory

Rats of the Dark Agouti strain were trained on delayed alternation under conditions that should encourage egocentric working memory. In two experiments a T-maze was set within a cross-maze so that different arms could be used for the sample and test runs. The maze had high opaque side-walls, and testing was conducted in low light levels so that distal visual cues might be eliminated. By rotating the maze 90° between the sample and choice run and by using two identical mazes set side by side it was possible to nullify other spatial strategies. Experiments 1 and 2 showed that rats preferentially used place information, intramaze cues, and direction cues, even though only egocentric or idiothetic (nonmatch-to-turn) working memory could successfully solve every trial. Rats were able to maintain an accurate sense of location within the maze even though distal cues were not visible and the animal was moved between the sample and choice runs. Experiment 2 confirmed that another rat strain (Long-Evans) shows the same learning profiles. Both experiments indicate that rats are very poor at using either egocentric or idiothetic information to alternate, and that retention delays as short as 10 s can eliminate the use of these forms of memory.